We are interested in understanding how plants use small proteins to dynamically adjust growth and development in response to environmental changes.
There is growing evidence that proteomes are more complex than previously anticipated. For instance, until recently, genes coding for proteins with fewer than 100 amino acids were often labeled as artefacts. As a result, many such small open reading frames were excluded in genome annotations. Moreover, in addition to these single, individual, open reading frames, small proteins can also arise through processes such as alternative splicing or alternative use of transcription start sites. Thus, one gene can code for more than one protein. These and other processes result in a much larger number of protein species in a given cell compared to the number of protein-coding genes in the genome.
In our research, we use both protein-centric approaches (starting with the identification and characterization of specific small proteins, often microProteins) and process-oriented approaches, where we try to understand how plants dynamically change their developmental decisions in response to environmental changes. To identify small proteins, such as microProteins in any sequenced genome, we developed miPFinder that can classify small proteins as microProteins (Fig. 1, Straub and Wenkel, 2017). Biological processes we study involve the promotion of growth in response to shading or the induction of flowering in response to day length and temperature. One of the things we have been able to show is that small B-box microProteins can strongly influence flowering (Fig.2 and Graeff et al., 2016).
The next steps
Owing to their small size and the predictability of protein interactions, microProteins are suitable for the regulation of biotechnological processes. With the help of new genome engineering tools, we are currently exploring the possibilities of generating microProteins de novo to control developmental pathways at will.
{tab=Team}- {tab=CV S. Wenkel}
- 2006: Dr. rer. nat. (genetics), University of Cologne/Max Planck Institute for Plant Breeding Research, Germany
- 2003: Diploma (M.Sc.) in Biology, University of Würzburg, Germany
- 02/2023: Professor, Umeå University, Sweden
- 2014-23: Associate professor, University of Copenhagen, Denmark
- 2009-14: Group Leader, Center for Plant Molecular Biology, University of Tübingen, Germany
- 2006-09: Postdoctoral Fellow, Carnegie Institution for Science, Stanford, USA
- 2003-06: PhD student, Max Planck Institute for Plant Breeding Research, Cologne, Germany
- 2013: ERC Starting Grant
- 2020: Novo Nordisk Ascending Investigator
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Paper doi link bibtex abstract
@article{vittozzi_abi5_2024, title = {{ABI5} binding proteins: key players in coordinating plant growth and development}, volume = {29}, issn = {1360-1385}, shorttitle = {{ABI5} binding proteins}, url = {https://www.sciencedirect.com/science/article/pii/S1360138524000657}, doi = {10.1016/j.tplants.2024.03.009}, abstract = {During the course of terrestrial evolution, plants have developed complex networks that involve the coordination of phytohormone signalling pathways in order to adapt to an ever-changing environment. Transcription factors coordinate these responses by engaging in different protein complexes and exerting both positive and negative effects. ABA INSENSITIVE 5 (ABI5) binding proteins (AFPs), which are closely related to NOVEL INTERACTOR OF JAZ (NINJA)-like proteins, are known for their fundamental role in plants’ morphological and physiological growth. Recent studies have shown that AFPs regulate several hormone-signalling pathways, including abscisic acid (ABA) and gibberellic acid (GA). Here, we review the genetic control of AFPs and their crosstalk with plant hormone signalling, and discuss the contributions of AFPs to plants’ growth and development.}, number = {9}, urldate = {2024-09-20}, journal = {Trends in Plant Science}, author = {Vittozzi, Ylenia and Krüger, Thorben and Majee, Adity and Née, Guillaume and Wenkel, Stephan}, month = sep, year = {2024}, keywords = {AFP (ABI5 binding protein), abscisic acid, flowering regulation, microprotein, seed germination}, pages = {1006--1017}, }
Paper doi link bibtex abstract
@article{petri_exploring_2024, title = {Exploring the world of small proteins in plant biology and bioengineering}, issn = {0168-9525}, url = {https://www.sciencedirect.com/science/article/pii/S0168952524002129}, doi = {10.1016/j.tig.2024.09.004}, abstract = {Small proteins are ubiquitous in all kingdoms of life. MicroProteins, initially characterized as small proteins with protein interaction domains that enable them to interact with larger multidomain proteins, frequently modulate the function of these proteins. The study of these small proteins has contributed to a greater comprehension of protein regulation. In addition to sequence homology, sequence-divergent small proteins have the potential to function as microProtein mimics, binding to structurally related proteins. Moreover, a multitude of other small proteins encoded by short open reading frames (sORFs) and peptides, derived from diverse sources such as long noncoding RNAs (lncRNAs) and miRNAs, contribute to a variety of biological processes. The potential of small proteins is evident, offering promising avenues for bioengineering that could revolutionize crop performance and reduce reliance on agrochemicals in future agriculture.}, urldate = {2024-10-18}, journal = {Trends in Genetics}, author = {Petri, Louise and Van Humbeeck, Anne and Niu, Huanying and Ter Waarbeek, Casper and Edwards, Ashleigh and Chiurazzi, Maurizio Junior and Vittozzi, Ylenia and Wenkel, Stephan}, month = oct, year = {2024}, keywords = {lncRNA, microProteins, sORFs, transcription factor}, }
Paper doi link bibtex abstract
@article{dusi_involvement_2024, title = {Involvement of the tomato {BBX16} and {BBX17} {microProteins} in reproductive development}, volume = {213}, issn = {0981-9428}, url = {https://www.sciencedirect.com/science/article/pii/S0981942824005412}, doi = {10.1016/j.plaphy.2024.108873}, abstract = {BBXs are B-Box zinc finger proteins that can act as transcription factors and regulators of protein complexes. Several BBX proteins play important roles in plant development. Two Arabidopsis thaliana microProteins belonging to the BBX family, named miP1a and miP1b, homotypically interact with and modulate the activity of other BBX proteins, including CONSTANS, which transcriptionally activates the florigen, FLOWERING LOCUS T. Arabidopsis plants overexpressing miP1a and miP1b showed delayed flowering. In tomato, the closest homologs of miP1a and miP1b are the microProteins SlBBX16 and SlBBX17. This study was aimed at investigating whether the constitutive expression of SlBBX16/17 in Arabidopsis and tomato impacted reproductive development. The heterologous expression of the two tomato microProteins in Arabidopsis caused a delay in the flowering transition; however, the effect was weaker than that observed when the native miP1a/b were overexpressed. In tomato, overexpression of SlBBX17 prolonged the flowering period; this effect was accompanied by downregulation of the flowering inhibitors Self Pruning (SP) and SP5G. SlBBX16 and SlBBX17 can hetero-oligomerize with TCMP-2, a cystine-knot peptide involved in flowering pattern regulation and early fruit development in tomato. The increased expression of both microProteins also caused alterations in tomato fruit development: we observed in the case of SlBBX17 a decrease in the number and size of ripe fruits as compared to WT plants, while for SlBBX16, a delay in fruit production up to the breaker stage. These effects were associated with changes in the expression of GA-responsive genes.}, urldate = {2024-07-01}, journal = {Plant Physiology and Biochemistry}, author = {Dusi, Valentina and Pennisi, Federica and Fortini, Daniela and Atarés, Alejandro and Wenkel, Stephan and Molesini, Barbara and Pandolfini, Tiziana}, month = aug, year = {2024}, keywords = {BBX, Flowering time, Fruit development, Gibberellins, MicroProteins}, pages = {108873}, }
Paper doi link bibtex abstract
@article{aguida_seeing_2024, title = {‘{Seeing}’ the electromagnetic spectrum: spotlight on the cryptochrome photocycle}, volume = {15}, issn = {1664-462X}, shorttitle = {‘{Seeing}’ the electromagnetic spectrum}, url = {https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2024.1340304}, doi = {10.3389/fpls.2024.1340304}, abstract = {Cryptochromes are widely dispersed flavoprotein photoreceptors that regulate numerous developmental responses to light in plants, as well as to stress and entrainment of the circadian clock in animals and humans. All cryptochromes are closely related to an ancient family of light-absorbing flavoenzymes known as photolyases, which use light as an energy source for DNA repair but themselves have no light sensing role. Here we review the means by which plant cryptochromes acquired a light sensing function. This transition involved subtle changes within the flavin binding pocket which gave rise to a visual photocycle consisting of light-inducible and dark-reversible flavin redox state transitions. In this photocycle, light first triggers flavin reduction from an initial dark-adapted resting state (FADox). The reduced state is the biologically active or ‘lit’ state, correlating with biological activity. Subsequently, the photoreduced flavin reoxidises back to the dark adapted or ‘resting’ state. Because the rate of reoxidation determines the lifetime of the signaling state, it significantly modulates biological activity. As a consequence of this redox photocycle Crys respond to both the wavelength and the intensity of light, but are in addition regulated by factors such as temperature, oxygen concentration, and cellular metabolites that alter rates of flavin reoxidation even independently of light. Mechanistically, flavin reduction is correlated with conformational change in the protein, which is thought to mediate biological activity through interaction with biological signaling partners. In addition, a second, entirely independent signaling mechanism arises from the cryptochrome photocycle in the form of reactive oxygen species (ROS). These are synthesized during flavin reoxidation, are known mediators of biotic and abiotic stress responses, and have been linked to Cry biological activity in plants and animals. Additional special properties arising from the cryptochrome photocycle include responsivity to electromagnetic fields and their applications in optogenetics. Finally, innovations in methodology such as the use of Nitrogen Vacancy (NV) diamond centers to follow cryptochrome magnetic field sensitivity in vivo are discussed, as well as the potential for a whole new technology of ‘magneto-genetics’ for future applications in synthetic biology and medicine.}, urldate = {2024-03-22}, journal = {Frontiers in Plant Science}, author = {Aguida, Blanche and Babo, Jonathan and Baouz, Soria and Jourdan, Nathalie and Procopio, Maria and El-Esawi, Mohamed A. and Engle, Dorothy and Mills, Stephen and Wenkel, Stephan and Huck, Alexander and Berg-Sørensen, Kirstine and Kampranis, Sotirios C. and Link, Justin and Ahmad, Margaret}, month = mar, year = {2024}, keywords = {⛔ No DOI found}, }
Paper doi link bibtex abstract
@article{heisler_context-specific_2022, title = {Context-specific functions of transcription factors controlling plant development: {From} leaves to flowers}, volume = {69}, issn = {1369-5266}, shorttitle = {Context-specific functions of transcription factors controlling plant development}, url = {https://www.sciencedirect.com/science/article/pii/S1369526622000917}, doi = {10.1016/j.pbi.2022.102262}, abstract = {Plant development is regulated by transcription factors that often act in more than one process and stage of development. Yet the molecular mechanisms that govern the functional diversity and specificity of these proteins remains far from understood. Flower development provides an ideal context to study these mechanisms since the development of distinct floral organs depends on similar but distinct combinations of transcriptional regulators. Recent work also highlights the importance of leaf polarity regulators as additional key factors in flower initiation, floral organ morphogenesis, and possibly floral organ positioning. A detailed understanding of how these factors work in combination will enable us to address outstanding questions in flower development including how distinct shapes and positions of floral organs are generated. Experimental approaches and computer-based modeling will be required to characterize gene-regulatory networks at the level of single cells.}, language = {en}, urldate = {2022-11-30}, journal = {Current Opinion in Plant Biology}, author = {Heisler, Marcus G. and Jönsson, Henrik and Wenkel, Stephan and Kaufmann, Kerstin}, month = oct, year = {2022}, pages = {102262}, }
Paper doi link bibtex abstract
@article{chiurazzi_controlling_2022, title = {Controlling flowering of {Medicago} sativa (alfalfa) by inducing dominant mutations}, volume = {64}, issn = {1744-7909}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/jipb.13186}, doi = {10.1111/jipb.13186}, abstract = {Breeding plants with polyploid genomes is challenging because functional redundancy hampers the identification of loss-of-function mutants. Medicago sativa is tetraploid and obligate outcrossing, which together with inbreeding depression complicates traditional breeding approaches in obtaining plants with a stable growth habit. Inducing dominant mutations would provide an alternative strategy to introduce domestication traits in plants with high gene redundancy. Here we describe two complementary strategies to induce dominant mutations in the M. sativa genome and how they can be relevant in the control of flowering time. First, we outline a genome-engineering strategy that harnesses the use of microProteins as developmental regulators. MicroProteins are small proteins that appeared during genome evolution from genes encoding larger proteins. Genome-engineering allows us to retrace evolution and create microProtein-coding genes de novo. Second, we provide an inventory of genes regulated by microRNAs that control plant development. Making respective gene transcripts microRNA-resistant by inducing point mutations can uncouple microRNA regulation. Finally, we investigated the recently published genomes of M. sativa and provide an inventory of breeding targets, some of which, when mutated, are likely to result in dominant traits.}, language = {en}, number = {2}, urldate = {2022-11-30}, journal = {Journal of Integrative Plant Biology}, author = {Chiurazzi, Maurizio Junior and Nørrevang, Anton Frisgaard and García, Pedro and Cerdán, Pablo D. and Palmgren, Michael and Wenkel, Stephan}, year = {2022}, keywords = {Medicago sativa, flowering time, genome-engineering, microProtein, microRNA}, pages = {205--214}, }
Paper doi link bibtex abstract
@article{sun_fiona1-mediated_2022, title = {{FIONA1}-mediated methylation of the 3’{UTR} of {FLC} affects {FLC} transcript levels and flowering in {Arabidopsis}}, volume = {18}, issn = {1553-7404}, url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1010386}, doi = {10.1371/journal.pgen.1010386}, abstract = {Adenosine bases of RNA can be transiently modified by the deposition of a methyl-group to form N6-methyladenosine (m6A). This adenosine-methylation is an ancient process and the enzymes involved are evolutionary highly conserved. A genetic screen designed to identify suppressors of late flowering transgenic Arabidopsis plants overexpressing the miP1a microProtein yielded a new allele of the FIONA1 (FIO1) m6A-methyltransferase. To characterize the early flowering phenotype of fio1 mutant plants we employed an integrative approach of mRNA-seq, Nanopore direct RNA-sequencing and meRIP-seq to identify differentially expressed transcripts as well as differentially methylated RNAs. We provide evidence that FIO1 is the elusive methyltransferase responsible for the 3’-end methylation of the FLOWERING LOCUS C (FLC) transcript. Furthermore, our genetic and biochemical data suggest that 3’-methylation stabilizes FLC mRNAs and non-methylated FLC is a target for rapid degradation.}, language = {en}, number = {9}, urldate = {2022-11-30}, journal = {PLOS Genetics}, author = {Sun, Bin and Bhati, Kaushal Kumar and Song, Peizhe and Edwards, Ashleigh and Petri, Louise and Kruusvee, Valdeko and Blaakmeer, Anko and Dolde, Ulla and Rodrigues, Vandasue and Straub, Daniel and Yang, Junbo and Jia, Guifang and Wenkel, Stephan}, month = sep, year = {2022}, keywords = {Arabidopsis thaliana, Flowering plants, Gene expression, Leaves, Messenger RNA, Methylation, Phenotypes, RNA sequencing}, pages = {e1010386}, }
Paper doi link bibtex abstract
@article{kruusvee_microproteins_2022, title = {Microproteins — lost in translation}, volume = {18}, copyright = {2022 Springer Nature America, Inc.}, issn = {1552-4469}, url = {https://www.nature.com/articles/s41589-022-01007-5}, doi = {10.1038/s41589-022-01007-5}, abstract = {Microproteins can be generated by a shift in the reading frame during translation. A chemoproteomics approach led to the identification of MINAS-60 as an alternative microprotein that regulates the assembly of the pre-60S ribosome.}, language = {en}, number = {6}, urldate = {2022-11-30}, journal = {Nature Chemical Biology}, author = {Kruusvee, Valdeko and Wenkel, Stephan}, month = jun, year = {2022}, keywords = {Nuclear organization, Proteins, Proteomics}, pages = {581--582}, }
Paper doi link bibtex abstract
@article{kruusvee_stop_2022, title = {Stop {CRYing}! {Inhibition} of cryptochrome function by small proteins}, volume = {50}, issn = {0300-5127}, url = {https://doi.org/10.1042/BST20190062}, doi = {10.1042/BST20190062}, abstract = {Plants can detect the presence of light using specialised photoreceptor proteins. These photoreceptors measure the intensity of light, but they can also respond to different spectra of light and thus ‘see' different colours. Cryptochromes, which are also present in animals, are flavin-based photoreceptors that enable plants to detect blue and ultraviolet-A (UV-A) light. In Arabidopsis, there are two cryptochromes, CRYPTOCHROME 1 (CRY1) and CRYPTOCHROME 2 (CRY2) with known sensory roles. They function in various processes such as blue-light mediated inhibition of hypocotyl elongation, photoperiodic promotion of floral initiation, cotyledon expansion, anthocyanin production, and magnetoreception, to name a few. In the dark, the cryptochromes are in an inactive monomeric state and undergo photochemical and conformational change in response to illumination. This results in flavin reduction, oligomerisation, and the formation of the ‘cryptochrome complexome'. Mechanisms of cryptochrome activation and signalling have been extensively studied and found to be conserved across phylogenetic lines. In this review, we will therefore focus on a far lesser-known mechanism of regulation that is unique to plant cryptochromes. This involves inhibition of cryptochrome activity by small proteins that prevent its dimerisation in response to light. The resulting inhibition of function cause profound alterations in economically important traits such as plant growth, flowering, and fruit production. This review will describe the known mechanisms of cryptochrome activation and signalling in the context of their modulation by these endogenous and artificial small inhibitor proteins. Promising new applications for biotechnological and agricultural applications will be discussed.}, number = {2}, urldate = {2022-11-30}, journal = {Biochemical Society Transactions}, author = {Kruusvee, Valdeko and Toft, Arendse Maria and Aguida, Blanche and Ahmad, Margaret and Wenkel, Stephan}, month = mar, year = {2022}, pages = {773--782}, }
Paper doi link bibtex abstract
@article{bresson_genetic_2022, title = {The genetic interaction of {REVOLUTA} and {WRKY53} links plant development, senescence, and immune responses}, volume = {17}, issn = {1932-6203}, url = {https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0254741}, doi = {10.1371/journal.pone.0254741}, abstract = {In annual plants, tight coordination of successive developmental events is of primary importance to optimize performance under fluctuating environmental conditions. The recent finding of the genetic interaction of WRKY53, a key senescence-related gene with REVOLUTA, a master regulator of early leaf patterning, raises the question of how early and late developmental events are connected. Here, we investigated the developmental and metabolic consequences of an alteration of the REVOLUTA and WRKY53 gene expression, from seedling to fruiting. Our results show that REVOLUTA critically controls late developmental phases and reproduction while inversely WRKY53 determines vegetative growth at early developmental stages. We further show that these regulators of distinct developmental phases frequently, but not continuously, interact throughout ontogeny and demonstrated that their genetic interaction is mediated by the salicylic acid (SA). Moreover, we showed that REVOLUTA and WRKY53 are keys regulatory nodes of development and plant immunity thought their role in SA metabolic pathways, which also highlights the role of REV in pathogen defence. Together, our findings demonstrate how late and early developmental events are tightly intertwined by molecular hubs. These hubs interact with each other throughout ontogeny, and participate in the interplay between plant development and immunity.}, language = {en}, number = {3}, urldate = {2022-11-30}, journal = {PLOS ONE}, author = {Bresson, Justine and Doll, Jasmin and Vasseur, François and Stahl, Mark and Roepenack-Lahaye, Edda von and Kilian, Joachim and Stadelhofer, Bettina and Kremer, James M. and Kolb, Dagmar and Wenkel, Stephan and Zentgraf, Ulrike}, month = mar, year = {2022}, keywords = {Arabidopsis thaliana, Flowering plants, Genetic interactions, Leaves, Metabolites, Plant development, Plant disease resistance, Plant pathogens}, pages = {e0254741}, }
Paper doi link bibtex abstract
@article{rodrigues_microprotein_2021, title = {A {microProtein} repressor complex in the shoot meristem controls the transition to flowering}, volume = {187}, issn = {0032-0889}, url = {https://doi.org/10.1093/plphys/kiab235}, doi = {10.1093/plphys/kiab235}, abstract = {MicroProteins are potent post-translational regulators. In Arabidopsis (Arabidopsis thaliana), the miP1a/b microProteins delay floral transition by forming a complex with CONSTANS (CO) and the co-repressor protein TOPLESS. To better understand the function of the miP1a microProtein in floral repression, we performed a genetic suppressor screen to identify suppressors of miP1a (sum) function. One mutant, sum1, exhibited strong suppression of the miP1a-induced late-flowering phenotype. Mapping of sum1 identified another allele of the gene encoding the histone H3K4 demethylase JUMONJI14 (JMJ14), which is required for miP1a function. Plants carrying mutations in JMJ14 exhibit an early flowering phenotype that is largely dependent on CO activity, supporting an additional role for CO in the repressive complex. We further investigated whether miP1a function involves chromatin modification, performed whole-genome methylome sequencing studies with plants ectopically expressing miP1a, and identified differentially methylated regions (DMRs). Among these DMRs is the promoter of FLOWERING LOCUS T (FT), the prime target of miP1a that is ectopically methylated in a JMJ14-dependent manner. Moreover, when aberrantly expressed at the shoot apex, CO induces early flowering, but only when JMJ14 is mutated. Detailed analysis of the genetic interaction among CO, JMJ14, miP1a/b, and TPL revealed a potential role for CO as a repressor of flowering in the shoot apical meristem (SAM). Altogether, our results suggest that a repressor complex operates in the SAM, likely to maintain it in an undifferentiated state until leaf-derived florigen signals induce SAM conversion into a floral meristem.}, number = {1}, urldate = {2022-11-30}, journal = {Plant Physiology}, author = {Rodrigues, Vandasue L. and Dolde, Ulla and Sun, Bin and Blaakmeer, Anko and Straub, Daniel and Eguen, Tenai and Botterweg-Paredes, Esther and Hong, Shinyoung and Graeff, Moritz and Li, Man-Wah and Gendron, Joshua M. and Wenkel, Stephan}, month = sep, year = {2021}, pages = {187--202}, }
Paper doi link bibtex
@article{bhati_microproteins_2021, title = {{MicroProteins}: {Expanding} functions and novel modes of regulation}, volume = {14}, issn = {1674-2052}, shorttitle = {{MicroProteins}}, url = {https://www.cell.com/molecular-plant/abstract/S1674-2052(21)00006-X}, doi = {10.1016/j.molp.2021.01.006}, language = {English}, number = {5}, urldate = {2022-11-30}, journal = {Molecular Plant}, author = {Bhati, Kaushal Kumar and Dolde, Ulla and Wenkel, Stephan}, month = may, year = {2021}, pages = {705--707}, }
Paper doi link bibtex abstract
@article{eguen_control_2020, title = {Control of flowering in rice through synthetic {microProteins}}, volume = {62}, issn = {1744-7909}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/jipb.12865}, doi = {10.1111/jipb.12865}, abstract = {Photoperiod-dependent flowering in rice is regulated by HEADING DATE 1 (Hd1), which acts as both an activator and repressor of flowering in a daylength-dependent manner. To investigate the use of microProteins as a tool to modify rice sensitivity to the photoperiod, we designed a synthetic Hd1 microProtein (Hd1miP) capable of interacting with Hd1 protein, and overexpressed it in rice. Transgenic OX-Hd1miP plants flowered significantly earlier than wild type plants when grown in non-inductive long day conditions. Our results show the potential of microProteins to serve as powerful tools for modulating crop traits and unraveling protein function.}, language = {en}, number = {6}, urldate = {2022-11-30}, journal = {Journal of Integrative Plant Biology}, author = {Eguen, Tenai and Ariza, Jorge Gomez and Brambilla, Vittoria and Sun, Bin and Bhati, Kaushal Kumar and Fornara, Fabio and Wenkel, Stephan}, year = {2020}, pages = {730--736}, }
Paper doi link bibtex abstract
@article{bhati_global_2020, title = {Global {Analysis} of {Cereal} {microProteins} {Suggests} {Diverse} {Roles} in {Crop} {Development} and {Environmental} {Adaptation}}, volume = {10}, issn = {2160-1836}, url = {https://doi.org/10.1534/g3.120.400794}, doi = {10.1534/g3.120.400794}, abstract = {MicroProteins are a class of small single-domain proteins that post-translationally regulate larger multidomain proteins from which they evolved or which they relate to. They disrupt the normal function of their targets by forming microProtein-target heterodimers through compatible protein-protein interaction (PPI) domains. Recent studies confirm the significance of microProteins in the fine-tuning of plant developmental processes such as shoot apical meristem maintenance and flowering time regulation. While there are a number of well-characterized microProteins in Arabidopsis thaliana, studies from more complex plant genomes are still missing. We have previously developed miPFinder, a software for identifying microProteins from annotated genomes. Here we present an improved version where we have updated the algorithm to increase its accuracy and speed, and used it to analyze five cereal crop genomes – wheat, rice, barley, maize and sorghum. We found 20,064 potential microProteins from a total of 258,029 proteins in these five organisms, of which approximately 2000 are high-confidence, i.e., likely to function as actual microProteins. Gene ontology analysis of these 2000 microProtein candidates revealed their roles in stress, light and growth responses, hormone signaling and transcriptional regulation. Using a recently developed rice gene co-expression database, we analyzed 347 potential rice microProteins that are also conserved in other cereal crops and found over 50 of these rice microProteins to be co-regulated with their identified interaction partners. Overall, our study reveals a rich source of biotechnologically interesting small proteins that regulate fundamental plant processes such a growth and stress response that could be utilized in crop bioengineering.}, number = {10}, urldate = {2022-11-30}, journal = {G3 Genes{\textbar}Genomes{\textbar}Genetics}, author = {Bhati, Kaushal Kumar and Kruusvee, Valdeko and Straub, Daniel and Chandran, Anil Kumar Nalini and Jung, Ki-Hong and Wenkel, Stephan}, month = oct, year = {2020}, pages = {3709--3717}, }
Paper doi link bibtex abstract
@article{hong_heterologous_2020, title = {Heterologous {microProtein} expression identifies {LITTLE} {NINJA}, a dominant regulator of jasmonic acid signaling}, volume = {117}, url = {https://www.pnas.org/doi/full/10.1073/pnas.2005198117}, doi = {10.1073/pnas.2005198117}, abstract = {MicroProteins are small, often single-domain proteins that are sequence-related to larger, often multidomain proteins. Here, we used a combination of comparative genomics and heterologous synthetic misexpression to isolate functional cereal microProtein regulators. Our approach identified LITTLE NINJA (LNJ), a microProtein that acts as a modulator of jasmonic acid (JA) signaling. Ectopic expression of LNJ in Arabidopsis resulted in stunted plants that resembled the decuple JAZ (jazD) mutant. In fact, comparing the transcriptomes of transgenic LNJ overexpressor plants and jazD revealed a large overlap of deregulated genes, suggesting that ectopic LNJ expression altered JA signaling. Transgenic Brachypodium plants with elevated LNJ expression levels showed deregulation of JA signaling as well and displayed reduced growth and enhanced production of side shoots (tiller). This tillering effect was transferable between grass species, and overexpression of LNJ in barley and rice caused similar traits. We used a clustered regularly interspaced short palindromic repeats (CRISPR) approach and created a LNJ-like protein in Arabidopsis by deleting parts of the coding sentence of the AFP2 gene that encodes a NINJA-domain protein. These afp2-crispr mutants were also stunted in size and resembled jazD. Thus, similar genome-engineering approaches can be exploited as a future tool to create LNJ proteins and produce cereals with altered architectures.}, number = {42}, urldate = {2022-11-30}, journal = {Proceedings of the National Academy of Sciences}, author = {Hong, Shin-Young and Sun, Bin and Straub, Daniel and Blaakmeer, Anko and Mineri, Lorenzo and Koch, Jonas and Brinch-Pedersen, Henrik and Holme, Inger B. and Burow, Meike and Lyngs Jørgensen, Hans Jørgen and Albà, M. Mar and Wenkel, Stephan}, month = oct, year = {2020}, pages = {26197--26205}, }
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@article{choi_light_2020, series = {Photobiology}, title = {Light {Triggers} the {miRNA}-{Biogenetic} {Inconsistency} for {De}-etiolated {Seedling} {Survivability} in {Arabidopsis} thaliana}, volume = {13}, issn = {1674-2052}, url = {https://www.sciencedirect.com/science/article/pii/S1674205219303375}, doi = {10.1016/j.molp.2019.10.011}, abstract = {The shift of dark-grown seedlings into light causes enormous transcriptome changes followed by a dramatic developmental transition. Here, we show that microRNA (miRNA) biogenesis also undergoes regulatory changes during de-etiolation. Etiolated seedlings maintain low levels of primary miRNAs (pri-miRNAs) and miRNA processing core proteins, such as Dicer-like 1, SERRATE, and HYPONASTIC LEAVES 1, whereas during de-etiolation both pri-miRNAs and the processing components accumulate to high levels. However, the levels of most miRNAs do not notably increase in response to light. To reconcile this inconsistency, we demonstrated that an unknown suppressor decreases miRNA-processing activity and light-induced SMALL RNA DEGRADING NUCLEASE 1 shortens the half-life of several miRNAs in de-etiolated seedlings. Taken together, these data suggest a novel mechanism, miRNA-biogenetic inconsistency, which accounts for the intricacy of miRNA biogenesis during de-etiolation. This mechanism is essential for the survival of de-etiolated seedlings after long-term skotomorphogenesis and their optimal adaptation to ever-changing light conditions.}, language = {en}, number = {3}, urldate = {2022-11-30}, journal = {Molecular Plant}, author = {Choi, Suk Won and Ryu, Moon Young and Viczián, András and Jung, Hyun Ju and Kim, Gu Min and Arce, Agustin L. and Achkar, Natalia P. and Manavella, Pablo and Dolde, Ulla and Wenkel, Stephan and Molnár, Attila and Nagy, Ferenc and Cho, Seok Keun and Yang, Seong Wook}, month = mar, year = {2020}, keywords = {Light signaling, miRNA biogenesis}, pages = {431--445}, }
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@article{botterweg-paredes_light_2020, title = {Light affects tissue patterning of the hypocotyl in the shade-avoidance response}, volume = {16}, issn = {1553-7404}, url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1008678}, doi = {10.1371/journal.pgen.1008678}, abstract = {Plants have evolved strategies to avoid shade and optimize the capture of sunlight. While some species are tolerant to shade, plants such as Arabidopsis thaliana are shade-intolerant and induce elongation of their hypocotyl to outcompete neighboring plants. We report the identification of a developmental module acting downstream of shade perception controlling vascular patterning. We show that Arabidopsis plants react to shade by increasing the number and types of water-conducting tracheary elements in the vascular cylinder to maintain vascular density constant. Mutations in genes affecting vascular patterning impair the production of additional xylem and also show defects in the shade-induced hypocotyl elongation response. Comparative analysis of the shade-induced transcriptomes revealed differences between wild type and vascular patterning mutants and it appears that the latter mutants fail to induce sets of genes encoding biosynthetic and cell wall modifying enzymes. Our results thus set the stage for a deeper understanding of how growth and patterning are coordinated in a dynamic environment.}, language = {en}, number = {3}, urldate = {2022-11-30}, journal = {PLOS Genetics}, author = {Botterweg-Paredes, Esther and Blaakmeer, Anko and Hong, Shin-Young and Sun, Bin and Mineri, Lorenzo and Kruusvee, Valdeko and Xie, Yakun and Straub, Daniel and Ménard, Delphine and Pesquet, Edouard and Wenkel, Stephan}, month = mar, year = {2020}, keywords = {Arabidopsis thaliana, Auxins, Gene expression, Genetically modified plants, Hypocotyl, Seedlings, Transcription factors, White light}, pages = {e1008678}, }
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@article{hong_multi-level_2020, title = {Multi-level analysis of the interactions between {REVOLUTA} and {MORE} {AXILLARY} {BRANCHES} 2 in controlling plant development reveals parallel, independent and antagonistic functions}, volume = {147}, issn = {0950-1991}, url = {https://doi.org/10.1242/dev.183681}, doi = {10.1242/dev.183681}, abstract = {Class III homeodomain leucine zipper (HD-ZIPIII) transcription factors play fundamental roles in controlling plant development. The known HD-ZIPIII target genes encode proteins involved in the production and dissipation of the auxin signal, HD-ZIPII transcription factors and components that feedback to regulate HD-ZIPIII expression or protein activity. Here, we have investigated the regulatory hierarchies of the control of MORE AXILLARY BRANCHES2 (MAX2) by the HD-ZIPIII protein REVOLUTA (REV). We found that REV can interact with the promoter of MAX2. In agreement, rev10D gain-of-function mutants had increased levels of MAX2 expression, while rev loss-of-function mutants showed lower levels of MAX2 in some tissues. Like REV, MAX2 plays known roles in the control of plant architecture, photobiology and senescence, which prompted us to initiate a multi-level analysis of growth phenotypes of hd-zipIII, max2 and respective higher order mutants thereof. Our data suggest a complex relationship of synergistic and antagonistic activities between REV and MAX2; these interactions appear to depend on the developmental context and do not all involve the direct regulation of MAX2 by REV.}, number = {10}, urldate = {2022-11-30}, journal = {Development}, author = {Hong, Shin-Young and Botterweg-Paredes, Esther and Doll, Jasmin and Eguen, Tenai and Blaakmeer, Anko and Matton, Sanne and Xie, Yakun and Skjøth Lunding, Bjørg and Zentgraf, Ulrike and Guan, Chunmei and Jiao, Yuling and Wenkel, Stephan}, month = may, year = {2020}, pages = {dev183681}, }
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@article{dehaan_roadmap_2020, title = {Roadmap for {Accelerated} {Domestication} of an {Emerging} {Perennial} {Grain} {Crop}}, volume = {25}, issn = {1360-1385}, url = {https://www.cell.com/trends/plant-science/abstract/S1360-1385(20)30053-4}, doi = {10.1016/j.tplants.2020.02.004}, language = {English}, number = {6}, urldate = {2022-11-30}, journal = {Trends in Plant Science}, author = {DeHaan, Lee and Larson, Steve and López-Marqués, Rosa L. and Wenkel, Stephan and Gao, Caixia and Palmgren, Michael}, month = jun, year = {2020}, keywords = {accelerated domestication, genome editing, perennial grain crops}, pages = {525--537}, }
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@article{yadav_b-box-containing_2019, title = {The {B}-{Box}-{Containing} {MicroProtein} {miP1a}/{BBX31} {Regulates} {Photomorphogenesis} and {UV}-{B} {Protection}}, volume = {179}, issn = {0032-0889}, url = {https://doi.org/10.1104/pp.18.01258}, doi = {10.1104/pp.18.01258}, abstract = {The bZIP transcription factor ELONGATED HYPOCOTYL5 (HY5) represents a major hub in the light-signaling cascade both under visible and UV-B light. The mode of transcriptional regulation of HY5, especially under UV-B light, is not well characterized. B-BOX (BBX) transcription factors regulate HY5 transcription and also posttranscriptionally modulate HY5 to control photomorphogenesis under white light. Here, we identify BBX31 as a key signaling intermediate in visible and UV-B light signal transduction in Arabidopsis (Arabidopsis thaliana). BBX31 expression is induced by UV-B radiation in a fluence-dependent manner. HY5 directly binds to the promoter of BBX31 and regulates its transcript levels. Loss- and gain-of-function mutants of BBX31 indicate that it acts as a negative regulator of photomorphogenesis under white light but is a positive regulator of UV-B signaling. Genetic interaction studies suggest that BBX31 regulates photomorphogenesis independent of HY5. We found no evidence for a direct BBX31-HY5 interaction, and they primarily regulate different sets of genes in white light. Under high doses of UV-B radiation, BBX31 promotes the accumulation of UV-protective flavonoids and phenolic compounds. It enhances tolerance to UV-B radiation by regulating genes involved in photoprotection and DNA repair in a HY5-dependent manner. Under UV-B radiation, overexpression of BBX31 enhances HY5 transcriptional levels in a UV RESISTANCE LOCUS8-dependent manner, suggesting that BBX31 might regulate HY5 transcription.}, number = {4}, urldate = {2022-11-30}, journal = {Plant Physiology}, author = {Yadav, Arpita and Bakshi, Souvika and Yadukrishnan, Premachandran and Lingwan, Maneesh and Dolde, Ulla and Wenkel, Stephan and Masakapalli, Shyam Kumar and Datta, Sourav}, month = apr, year = {2019}, pages = {1876--1892}, }
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@article{bhati_approaches_2018, title = {Approaches to identify and characterize {microProteins} and their potential uses in biotechnology}, volume = {75}, issn = {1420-9071}, url = {https://doi.org/10.1007/s00018-018-2818-8}, doi = {10.1007/s00018-018-2818-8}, abstract = {MicroProteins are small proteins that contain a single protein domain and are related to larger, often multi-domain proteins. At the molecular level, microProteins act by interfering with the formation of higher order protein complexes. In the past years, several microProteins have been identified in plants and animals that strongly influence biological processes. Due to their ability to act as dominant regulators in a targeted manner, microProteins have a high potential for biotechnological use. In this review, we present different ways in which microProteins are generated and we elaborate on techniques used to identify and characterize them. Finally, we give an outlook on possible applications in biotechnology.}, language = {en}, number = {14}, urldate = {2022-11-30}, journal = {Cellular and Molecular Life Sciences}, author = {Bhati, Kaushal Kumar and Blaakmeer, Anko and Paredes, Esther Botterweg and Dolde, Ulla and Eguen, Tenai and Hong, Shin-Young and Rodrigues, Vandasue and Straub, Daniel and Sun, Bin and Wenkel, Stephan}, month = jul, year = {2018}, keywords = {Complex, Inhibition, MiPFinder, MicroProtein, Protein–protein interaction, Small proteins, Targets}, pages = {2529--2536}, }
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@article{zhang_spatiotemporal_2018, title = {Spatiotemporal control of axillary meristem formation by interacting transcriptional regulators}, volume = {145}, issn = {0950-1991}, url = {https://doi.org/10.1242/dev.158352}, doi = {10.1242/dev.158352}, abstract = {Branching is a common feature of plant development. In seed plants, axillary meristems (AMs) initiate in leaf axils to enable lateral shoot branching. AM initiation requires a high level of expression of the meristem marker SHOOT MERISTEMLESS (STM) in the leaf axil. Here, we show that modules of interacting transcriptional regulators control STM expression and AM initiation. Two redundant AP2-type transcription factors, DORNRÖSCHEN (DRN) and DORNRÖSCHEN-LIKE (DRNL), control AM initiation by regulating STM expression. DRN and DRNL directly upregulate STM expression in leaf axil meristematic cells, as does another transcription factor, REVOLUTA (REV). The activation of STM expression by DRN/DRNL depends on REV, and vice versa. DRN/DRNL and REV have overlapping expression patterns and protein interactions in the leaf axil, which are required for the upregulation of STM expression. Furthermore, LITTLE ZIPPER3, another REV-interacting protein, is expressed in the leaf axil and interferes with the DRN/DRNL-REV interaction to negatively modulate STM expression. Our results support a model in which interacting transcriptional regulators fine-tune the expression of STM to precisely regulate AM initiation. Thus, shoot branching recruits the same conserved protein complexes used in embryogenesis and leaf polarity patterning.}, number = {24}, urldate = {2022-11-30}, journal = {Development}, author = {Zhang, Cui and Wang, Jin and Wenkel, Stephan and Chandler, John W. and Werr, Wolfgang and Jiao, Yuling}, month = dec, year = {2018}, pages = {dev158352}, }
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@article{dolde_synthetic_2018, title = {Synthetic {MicroProteins}: {Versatile} {Tools} for {Posttranslational} {Regulation} of {Target} {Proteins}}, volume = {176}, issn = {0032-0889}, shorttitle = {Synthetic {MicroProteins}}, url = {https://doi.org/10.1104/pp.17.01743}, doi = {10.1104/pp.17.01743}, abstract = {MicroProteins are small, single-domain proteins that regulate multidomain proteins by sequestering them into novel, often nonproductive, complexes. Several microProteins have been identified in plants and animals, most of which negatively regulate transcription factors. MicroProtein candidates that potentially target a wide range of different protein classes were recently identified in a computational approach. Here, we classified all Arabidopsis (Arabidopsis thaliana) microProteins and developed a synthetic microProtein approach to target specific protein classes, such as hydrolases, receptors, and lyases, in a proof-of-concept approach. Our findings reveal that microProteins can be used to influence different physiological processes, which makes them useful tools for posttranslational regulation in plants and potentially also in animals.}, number = {4}, urldate = {2022-11-30}, journal = {Plant Physiology}, author = {Dolde, Ulla and Rodrigues, Vandasue and Straub, Daniel and Bhati, Kaushal Kumar and Choi, Sukwon and Yang, Seong Wook and Wenkel, Stephan}, month = apr, year = {2018}, pages = {3136--3145}, }
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@article{straub_cross-species_2017, title = {Cross-{Species} {Genome}-{Wide} {Identification} of {Evolutionary} {Conserved} {MicroProteins}}, volume = {9}, issn = {1759-6653}, url = {https://doi.org/10.1093/gbe/evx041}, doi = {10.1093/gbe/evx041}, abstract = {MicroProteins are small single-domain proteins that act by engaging their targets into different, sometimes nonproductive protein complexes. In order to identify novel microProteins in any sequenced genome of interest, we have developed miPFinder, a program that identifies and classifies potential microProteins. In the past years, several microProteins have been discovered in plants where they are mainly involved in the regulation of development by fine-tuning transcription factor activities. The miPFinder algorithm identifies all up to date known plant microProteins and extends the microProtein concept beyond transcription factors to other protein families. Here, we reveal potential microProtein candidates in several plant and animal reference genomes. A large number of these microProteins are species-specific while others evolved early and are evolutionary highly conserved. Most known microProtein genes originated from large ancestral genes by gene duplication, mutation and subsequent degradation. Gene ontology analysis shows that putative microProtein ancestors are often located in the nucleus, and involved in DNA binding and formation of protein complexes. Additionally, microProtein candidates act in plant transcriptional regulation, signal transduction and anatomical structure development. MiPFinder is freely available to find microProteins in any genome and will aid in the identification of novel microProteins in plants and animals.}, number = {3}, urldate = {2022-11-30}, journal = {Genome Biology and Evolution}, author = {Straub, Daniel and Wenkel, Stephan}, month = mar, year = {2017}, pages = {777--789}, }
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@article{barghetti_heat-shock_2017, title = {Heat-shock protein 40 is the key farnesylation target in meristem size control, abscisic acid signaling, and drought resistance}, volume = {31}, issn = {0890-9369, 1549-5477}, url = {http://genesdev.cshlp.org/content/31/22/2282}, doi = {10.1101/gad.301242.117}, abstract = {Protein farnesylation is central to molecular cell biology. In plants, protein farnesyl transferase mutants are pleiotropic and exhibit defective meristem organization, hypersensitivity to the hormone abscisic acid, and increased drought resistance. The precise functions of protein farnesylation in plants remain incompletely understood because few relevant farnesylated targets have been identified. Here, we show that defective farnesylation of a single factor—heat-shock protein 40 (HSP40), encoded by the J2 and J3 genes—is sufficient to confer ABA hypersensitivity, drought resistance, late flowering, and enlarged meristems, indicating that altered function of chaperone client proteins underlies most farnesyl transferase mutant phenotypes. We also show that expression of an abiotic stress-related microRNA (miRNA) regulon controlled by the transcription factor SPL7 requires HSP40 farnesylation. Expression of a truncated SPL7 form mimicking its activated proteolysis fragment of the membrane-bound SPL7 precursor partially restores accumulation of SPL7-dependent miRNAs in farnesyl transferase mutants. These results implicate the pathway directing SPL7 activation from its membrane-bound precursor as an important target of farnesylated HSP40, consistent with our demonstration that HSP40 farnesylation facilitates its membrane association. The results also suggest that altered gene regulation via select miRNAs contributes to abiotic stress-related phenotypes of farnesyl transferase mutants.}, language = {en}, number = {22}, urldate = {2022-11-30}, journal = {Genes \& Development}, author = {Barghetti, Andrea and Sjögren, Lars and Floris, Maïna and Paredes, Esther Botterweg and Wenkel, Stephan and Brodersen, Peter}, month = nov, year = {2017}, keywords = {Arabidopsis, abscisic acid, drought resistance, farnesylation, heat-shock proteins, meristem, microRNAs}, pages = {2282--2295}, }
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@article{merelo_shady_2017, series = {35 {Growth} and development 2017}, title = {The shady side of leaf development: the role of the {REVOLUTA}/{KANADI1} module in leaf patterning and auxin-mediated growth promotion}, volume = {35}, issn = {1369-5266}, shorttitle = {The shady side of leaf development}, url = {https://www.sciencedirect.com/science/article/pii/S1369526616302114}, doi = {10.1016/j.pbi.2016.11.016}, abstract = {Leaves are present in all land plants and are specialized organs for light harvesting. They arise at the flanks of the shoot apical meristem (SAM), and develop into lamina structures that exhibit adaxial/abaxial (upper/lower side of the leaf) polarity. At the molecular level, an intricate regulatory network determines ad-/abaxial polarity in Arabidopsis thaliana leaves, where the Class III Homeodomain Leucine Zipper (HD-ZIPIII) and KANADI (KAN) proteins are key mediators. The HD-ZIPIII REVOLUTA (REV) is expressed in the adaxial domain of lateral organs, whereas KAN1 is involved in abaxial differentiation. The REV/KAN1 module directly and antagonistically regulates the expression of several genes involved in shade-induced growth and auxin biosynthetic enzymes.}, language = {en}, urldate = {2022-11-30}, journal = {Current Opinion in Plant Biology}, author = {Merelo, Paz and Paredes, Esther Botterweg and Heisler, Marcus G and Wenkel, Stephan}, month = feb, year = {2017}, pages = {111--116}, }
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@article{graeff_microprotein-mediated_2016, title = {{MicroProtein}-{Mediated} {Recruitment} of {CONSTANS} into a {TOPLESS} {Trimeric} {Complex} {Represses} {Flowering} in {Arabidopsis}}, volume = {12}, issn = {1553-7404}, url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1005959}, doi = {10.1371/journal.pgen.1005959}, abstract = {MicroProteins are short, single domain proteins that act by sequestering larger, multi-domain proteins into non-functional complexes. MicroProteins have been identified in plants and animals, where they are mostly involved in the regulation of developmental processes. Here we show that two Arabidopsis thaliana microProteins, miP1a and miP1b, physically interact with CONSTANS (CO) a potent regulator of flowering time. The miP1a/b-type microProteins evolved in dicotyledonous plants and have an additional carboxy-terminal PF(V/L)FL motif. This motif enables miP1a/b microProteins to interact with TOPLESS/TOPLESS-RELATED (TPL/TPR) proteins. Interaction of CO with miP1a/b/TPL causes late flowering due to a failure in the induction of FLOWERING LOCUS T (FT) expression under inductive long day conditions. Both miP1a and miP1b are expressed in vascular tissue, where CO and FT are active. Genetically, miP1a/b act upstream of CO thus our findings unravel a novel layer of flowering time regulation via microProtein-inhibition.}, language = {en}, number = {3}, urldate = {2022-11-30}, journal = {PLOS Genetics}, author = {Graeff, Moritz and Straub, Daniel and Eguen, Tenai and Dolde, Ulla and Rodrigues, Vandasue and Brandt, Ronny and Wenkel, Stephan}, month = mar, year = {2016}, keywords = {Arabidopsis thaliana, Flowering plants, Gene expression, Genetically modified plants, Leaves, Protein domains, Transcription factors, Yeast}, pages = {e1005959}, }
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@article{merelo_regulation_2016, title = {Regulation of {MIR165}/166 by class {II} and class {III} homeodomain leucine zipper proteins establishes leaf polarity}, volume = {113}, url = {https://www.pnas.org/doi/10.1073/pnas.1516110113}, doi = {10.1073/pnas.1516110113}, abstract = {A defining feature of plant leaves is their flattened shape. This shape depends on an antagonism between the genes that specify adaxial (top) and abaxial (bottom) tissue identity; however, the molecular nature of this antagonism remains poorly understood. Class III homeodomain leucine zipper (HD-ZIP) transcription factors are key mediators in the regulation of adaxial–abaxial patterning. Their expression is restricted adaxially during early development by the abaxially expressed microRNA (MIR)165/166, yet the mechanism that restricts MIR165/166 expression to abaxial leaf tissues remains unknown. Here, we show that class III and class II HD-ZIP proteins act together to repress MIR165/166 via a conserved cis-element in their promoters. Organ morphology and tissue patterning in plants, therefore, depend on a bidirectional repressive circuit involving a set of miRNAs and its targets.}, number = {42}, urldate = {2022-11-30}, journal = {Proceedings of the National Academy of Sciences}, author = {Merelo, Paz and Ram, Hathi and Pia Caggiano, Monica and Ohno, Carolyn and Ott, Felix and Straub, Daniel and Graeff, Moritz and Cho, Seok Keun and Yang, Seong Wook and Wenkel, Stephan and Heisler, Marcus G.}, month = oct, year = {2016}, pages = {11973--11978}, }
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@article{xie_meta-analysis_2015, title = {Meta-{Analysis} of {Arabidopsis} {KANADI1} {Direct} {Target} {Genes} {Identifies} a {Basic} {Growth}-{Promoting} {Module} {Acting} {Upstream} of {Hormonal} {Signaling} {Pathways}}, volume = {169}, issn = {0032-0889}, url = {https://doi.org/10.1104/pp.15.00764}, doi = {10.1104/pp.15.00764}, abstract = {An intricate network of antagonistically acting transcription factors mediates the formation of a flat leaf lamina of Arabidopsis (Arabidopsis thaliana) plants. In this context, members of the class III homeodomain leucine zipper (HD-ZIPIII) transcription factor family specify the adaxial domain (future upper side) of the leaf, while antagonistically acting KANADI transcription factors determine the abaxial domain (future lower side). Here, we used a messenger RNA sequencing approach to identify genes regulated by KANADI1 (KAN1) and subsequently performed a meta-analysis combining our data sets with published genome-wide data sets. Our analysis revealed that KAN1 acts upstream of several genes encoding auxin biosynthetic enzymes. When exposed to shade, we found three YUCCA genes, YUC2, YUC5, and YUC8, to be transcriptionally up-regulated, which correlates with an increase in the levels of free auxin. When ectopically expressed, KAN1 is able to transcriptionally repress these three YUC genes and thereby block shade-induced auxin biosynthesis. Consequently, KAN1 is able to strongly suppress shade-avoidance responses. Taken together, we hypothesize that HD-ZIPIII/KAN form the basis of a basic growth-promoting module. Hypocotyl extension in the shade and outgrowth of new leaves both involve auxin synthesis and signaling, which are under the direct control of HD-ZIPIII/KAN.}, number = {2}, urldate = {2022-11-30}, journal = {Plant Physiology}, author = {Xie, Yakun and Straub, Daniel and Eguen, Tenai and Brandt, Ronny and Stahl, Mark and Martínez-García, Jaime F. and Wenkel, Stephan}, month = oct, year = {2015}, pages = {1240--1253}, }
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@article{eguen_microproteins_2015, title = {{MicroProteins}: small size – big impact}, volume = {20}, issn = {1360-1385}, shorttitle = {{MicroProteins}}, url = {https://www.cell.com/trends/plant-science/abstract/S1360-1385(15)00140-5}, doi = {10.1016/j.tplants.2015.05.011}, language = {English}, number = {8}, urldate = {2022-11-30}, journal = {Trends in Plant Science}, author = {Eguen, Tenai and Straub, Daniel and Graeff, Moritz and Wenkel, Stephan}, month = aug, year = {2015}, keywords = {MicroProteins, dominant-negative effect, modulatory regulation, non-functional complexes, short single domain, transcription factor regulation}, pages = {477--482}, }
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@article{brandt_homeodomain_2014, title = {Homeodomain leucine-zipper proteins and their role in synchronizing growth and development with the environment}, volume = {56}, issn = {1744-7909}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/jipb.12185}, doi = {10.1111/jipb.12185}, abstract = {The Arabidopsis (Arabidopsis thaliana L.) genome encodes for four distinct classes of homeodomain leucine-zipper (HD-ZIP) transcription factors (HD-ZIPI to HD-ZIPIV), which are all organized in multi-gene families. HD-ZIP transcription factors act as sequence-specific DNA-binding proteins that are able to control the expression level of target genes. While HD-ZIPI and HD-ZIPII proteins are mainly associated with environmental responses, HD-ZIPIII and HD-ZIPIV are primarily known to act as patterning factors. Recent studies have challenged this view. It appears that several of the different HD-ZIP families interact genetically to align both morphogenesis and environmental responses, most likely by modulating phytohormone-signaling networks.}, language = {en}, number = {6}, urldate = {2022-11-30}, journal = {Journal of Integrative Plant Biology}, author = {Brandt, Ronny and Cabedo, Marc and Xie, Yakun and Wenkel, Stephan}, year = {2014}, keywords = {KANADI, REVOLUTA, Transcription factors, abscisic acid, auxin, homeodomain, leaf development, leucine zipper, light signaling, microRNA, water stress}, pages = {518--526}, }
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@article{xie_revoluta_2014, title = {{REVOLUTA} and {WRKY53} connect early and late leaf development in {Arabidopsis}}, volume = {141}, issn = {0950-1991}, url = {https://doi.org/10.1242/dev.117689}, doi = {10.1242/dev.117689}, abstract = {As sessile organisms, plants have to continuously adjust growth and development to ever-changing environmental conditions. At the end of the growing season, annual plants induce leaf senescence to reallocate nutrients and energy-rich substances from the leaves to the maturing seeds. Thus, leaf senescence is a means with which to increase reproductive success and is therefore tightly coupled to the developmental age of the plant. However, senescence can also be induced in response to sub-optimal growth conditions as an exit strategy, which is accompanied by severely reduced yield. Here, we show that class III homeodomain leucine zipper (HD-ZIPIII) transcription factors, which are known to be involved in basic pattern formation, have an additional role in controlling the onset of leaf senescence in Arabidopsis. Several potential direct downstream genes of the HD-ZIPIII protein REVOLUTA (REV) have known roles in environment-controlled physiological processes. We report that REV acts as a redox-sensitive transcription factor, and directly and positively regulates the expression of WRKY53, a master regulator of age-induced leaf senescence. HD-ZIPIII proteins are required for the full induction of WRKY53 in response to oxidative stress, and mutations in HD-ZIPIII genes strongly delay the onset of senescence. Thus, a crosstalk between early and late stages of leaf development appears to contribute to reproductive success.}, number = {24}, urldate = {2022-11-30}, journal = {Development}, author = {Xie, Yakun and Huhn, Kerstin and Brandt, Ronny and Potschin, Maren and Bieker, Stefan and Straub, Daniel and Doll, Jasmin and Drechsler, Thomas and Zentgraf, Ulrike and Wenkel, Stephan}, month = dec, year = {2014}, pages = {4772--4783}, }
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@article{brandt_control_2013, series = {Developmental plasticity and adaptation in plants}, title = {Control of stem cell homeostasis via interlocking {microRNA} and {microProtein} feedback loops}, volume = {130}, issn = {0925-4773}, url = {https://www.sciencedirect.com/science/article/pii/S0925477312000603}, doi = {10.1016/j.mod.2012.06.007}, abstract = {Stem cells in the shoot apex of plants produce cells required for the formation of new leaves. Adult leaves are composed of multiple tissue layers arranged along the dorso-ventral (adaxial/abaxial) axis. Class III homeodomain leucine zipper (HD-ZIPIII) transcription factors play an important role in the set-up of leaf polarity in plants. Loss of HD-ZIPIII function results in strongly misshapen leaves and in severe cases fosters the consumption of the apical stem cells, thus causing a growth arrest in mutant plants. HD-ZIPIII mRNA is under tight control by microRNAs 165/166. In addition to the microRNA-action a second layer of regulation is established by LITTLE ZIPPER (ZPR)-type microProteins, which can interact with HD-ZIPIII proteins, forming attenuated protein complexes. Here we show that REVOLUTA (REV, a member of the HD-ZIPIII family) directly regulates the expression of ARGONAUTE10 (AGO10), ZPR1 and ZPR3. Because AGO10 was shown to dampen microRNA165/6 function, REV establishes a positive feedback loop on its own activity. Since ZPR-type microProteins are known to reduce HD-ZIPIII protein activity, REV concomitantly establishes a negative feedback loop. We propose that the interconnection of these microRNA/microProtein feedback loops regulates polarity set-up and stem cell activity in plants.}, language = {en}, number = {1}, urldate = {2022-11-30}, journal = {Mechanisms of Development}, author = {Brandt, Ronny and Xie, Yakun and Musielak, Thomas and Graeff, Moritz and Stierhof, York-Dieter and Huang, Hai and Liu, Chun-Ming and Wenkel, Stephan}, month = jan, year = {2013}, keywords = {AGO10, HD-ZIPIII transcription factors, LITTLE ZIPPER, Shoot apical meristem, microProteins, microRNAs}, pages = {25--33}, }
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@article{merelo_genome-wide_2013, title = {Genome-{Wide} {Identification} of {KANADI1} {Target} {Genes}}, volume = {8}, issn = {1932-6203}, url = {https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0077341}, doi = {10.1371/journal.pone.0077341}, abstract = {Plant organ development and polarity establishment is mediated by the action of several transcription factors. Among these, the KANADI (KAN) subclade of the GARP protein family plays important roles in polarity-associated processes during embryo, shoot and root patterning. In this study, we have identified a set of potential direct target genes of KAN1 through a combination of chromatin immunoprecipitation/DNA sequencing (ChIP-Seq) and genome-wide transcriptional profiling using tiling arrays. Target genes are over-represented for genes involved in the regulation of organ development as well as in the response to auxin. KAN1 affects directly the expression of several genes previously shown to be important in the establishment of polarity during lateral organ and vascular tissue development. We also show that KAN1 controls through its target genes auxin effects on organ development at different levels: transport and its regulation, and signaling. In addition, KAN1 regulates genes involved in the response to abscisic acid, jasmonic acid, brassinosteroids, ethylene, cytokinins and gibberellins. The role of KAN1 in organ polarity is antagonized by HD-ZIPIII transcription factors, including REVOLUTA (REV). A comparison of their target genes reveals that the REV/KAN1 module acts in organ patterning through opposite regulation of shared targets. Evidence of mutual repression between closely related family members is also shown.}, language = {en}, number = {10}, urldate = {2022-11-30}, journal = {PLOS ONE}, author = {Merelo, Paz and Xie, Yakun and Brand, Lucas and Ott, Felix and Weigel, Detlef and Bowman, John L. and Heisler, Marcus G. and Wenkel, Stephan}, month = oct, year = {2013}, keywords = {Auxins, DNA transcription, Gene expression, Gene regulation, Leaves, Organogenesis, Transcription factors, Transcriptional control}, pages = {e77341}, }
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@article{bou-torrent_athb4_2012, title = {{ATHB4} and {HAT3}, two class {II} {HD}-{ZIP} transcription factors, control leaf development in {Arabidopsis}}, volume = {7}, issn = {null}, url = {https://doi.org/10.4161/psb.21824}, doi = {10.4161/psb.21824}, abstract = {In response to plant proximity or canopy shade, plants can react by altering elongation growth and development. Several members of the class II homeodomain-leucine zipper (HD-ZIPII) transcription factor family have been shown to play an instrumental role in the responses to shade. HD-ZIP members of the class III (HD-ZIPIII), by contrast, are involved in basic patterning processes. We recently showed that REVOLUTA (REV), a member of the HD-ZIPIII family, directly and positively regulates the expression of several genes involved in shade-induced growth, such as those encoding HD-ZIPII factors HAT2, HAT3, ATHB2/HAT4 and ATHB4, and of the components of the auxin biosynthesis pathway YUCCA5 and TAA1. Furthermore, we could demonstrate a novel role for HD-ZIPIII in shade-induced promotion of growth. Here we show that besides responding to shade, ATHB4 and HAT3 have a critical role in establishing the dorso-ventral axis in cotyledons and developing leaves. Loss-of-function mutations in these two HD-ZIPII genes (athb4 hat3) results in severely abaxialized, entirely radialized leaves. Conversely, overexpression of HAT3 results in adaxialized leaf development. Taken together, our findings unravel a so far unappreciated role for an HD-ZIPII/HD-ZIPIII module required for dorso-ventral patterning of leaves. The finding that HD-ZIPII/HD-ZIPIII also function in shade avoidance suggests that this module is at the nexus of patterning and growth promotion.}, number = {11}, urldate = {2022-11-30}, journal = {Plant Signaling \& Behavior}, author = {Bou-Torrent, Jordi and Salla-Martret, Mercè and Brandt, Ronny and Musielak, Thomas and Palauqui, Jean-Christophe and Martínez-García, Jaime F. and Wenkel, Stephan}, month = nov, year = {2012}, keywords = {Arabidopsis thaliana, HD-ZIPII, HD-ZIPIII, auxin, leaf development, shade avoidance}, pages = {1382--1387}, }
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@article{gendron_brassinosteroids_2012, title = {Brassinosteroids regulate organ boundary formation in the shoot apical meristem of {Arabidopsis}}, volume = {109}, url = {https://www.pnas.org/doi/full/10.1073/pnas.1210799110}, doi = {10.1073/pnas.1210799110}, abstract = {Spatiotemporal control of the formation of organ primordia and organ boundaries from the stem cell niche in the shoot apical meristem (SAM) determines the patterning and architecture of plants, but the underlying signaling mechanisms remain poorly understood. Here we show that brassinosteroids (BRs) play a key role in organ boundary formation by repressing organ boundary identity genes. BR-hypersensitive mutants display organ-fusion phenotypes, whereas BR-insensitive mutants show enhanced organ boundaries. The BR-activated transcription factor BZR1 directly represses the CUP-SHAPED COTYLEDON (CUC) family of organ boundary identity genes. In WT plants, BZR1 accumulates at high levels in the nuclei of central meristem and organ primordia but at a low level in organ boundary cells to allow CUC gene expression. Activation of BR signaling represses CUC gene expression and causes organ fusion phenotypes. This study uncovers a role for BR in the spatiotemporal control of organ boundary formation and morphogenesis in the SAM.}, number = {51}, urldate = {2022-11-30}, journal = {Proceedings of the National Academy of Sciences}, author = {Gendron, Joshua M. and Liu, Jiang-Shu and Fan, Min and Bai, Ming-Yi and Wenkel, Stephan and Springer, Patricia S. and Barton, M. Kathryn and Wang, Zhi-Yong}, month = dec, year = {2012}, pages = {21152--21157}, }
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@article{brandt_genome-wide_2012, title = {Genome-wide binding-site analysis of {REVOLUTA} reveals a link between leaf patterning and light-mediated growth responses}, volume = {72}, issn = {1365-313X}, doi = {10/f3srjk}, abstract = {Unlike the situation in animals, the final morphology of the plant body is highly modulated by the environment. During Arabidopsis development, intrinsic factors provide the framework for basic patterning processes. CLASS III HOMEODOMAIN LEUCINE ZIPPER (HD-ZIPIII) transcription factors are involved in embryo, shoot and root patterning. During vegetative growth HD-ZIPIII proteins control several polarity set-up processes such as in leaves and the vascular system. We have identified several direct target genes of the HD-ZIPIII transcription factor REVOLUTA (REV) using a chromatin immunoprecipitation/DNA sequencing (ChIP-Seq) approach. This analysis revealed that REV acts upstream of auxin biosynthesis and affects directly the expression of several class II HD-ZIP transcription factors that have been shown to act in the shade-avoidance response pathway. We show that, as well as involvement in basic patterning, HD-ZIPIII transcription factors have a critical role in the control of the elongation growth that is induced when plants experience shade. Leaf polarity is established by the opposed actions of HD-ZIPIII and KANADI transcription factors. Finally, our study reveals that the module that consists of HD-ZIPIII/KANADI transcription factors controls shade growth antagonistically and that this antagonism is manifested in the opposed regulation of shared target genes.}, language = {eng}, number = {1}, journal = {The Plant Journal: For Cell and Molecular Biology}, author = {Brandt, Ronny and Salla-Martret, Mercè and Bou-Torrent, Jordi and Musielak, Thomas and Stahl, Mark and Lanz, Christa and Ott, Felix and Schmid, Markus and Greb, Thomas and Schwarz, Martina and Choi, Sang-Bong and Barton, M. Kathryn and Reinhart, Brenda J. and Liu, Tie and Quint, Marcel and Palauqui, Jean-Christophe and Martínez-García, Jaime F. and Wenkel, Stephan}, month = oct, year = {2012}, keywords = {Adaptation, Physiological, Arabidopsis, Arabidopsis Proteins, Arabidopsis thaliana, Binding Sites, Body Patterning, Chromatin Immunoprecipitation, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Genome, Plant, HD-ZIPII, HD-ZIPIII, Homeodomain Proteins, Hypocotyl, In Situ Hybridization, Indoleacetic Acids, Light, Mutation, Phylogeny, Plant Leaves, Sequence Analysis, DNA, Signal Transduction, Transcription Factors, auxin, leaf development, shade avoidance}, pages = {31--42}, }
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@article{graeff_regulation_2012, title = {Regulation of protein function by interfering protein species}, volume = {3}, issn = {1868-503X}, url = {https://www.degruyter.com/document/doi/10.1515/bmc.2011.053/html?lang=en}, doi = {10.1515/bmc.2011.053}, abstract = {Most proteins do not function alone but act in protein complexes. For several transcriptional regulators, it is known that they have to homo- or heterodimerize prior to DNA binding. These protein interactions occur through defined protein-protein-interaction (PPI) domains. More than two decades ago, inhibitor of DNA binding (ID), a small protein containing a single helix-loop-helix (HLH) motif was identified. ID is able to interact with the larger DNA-binding basic helix-loop-helix (bHLH) transcription factors, but due to the lack of the basic domain required for DNA binding, ID traps bHLH proteins in non-functional complexes. Work in plants has, in the recent years, identified more small proteins acting in analogy to ID. A hallmark of these small negative acting proteins is the presence of a protein-interaction domain and the absence of other functional domains required for transcriptional activation or DNA binding. Because these proteins are often very small and function in analogy to microRNAs (meaning in a dominant-negative manner), we propose to refer to these protein species as ‘microProteins’ (miPs). miPs can be encoded in the genome as individual transcription units but can also be produced by alternative splicing. Other negatively acting proteins, consisting of more than one domain, have also been identified, and we propose to call these proteins ‘interfering proteins’ (iPs). The aim of this review is to state more precisely how to discriminate miPs from iPs. Therefore, we will highlight recent findings on both protein species and describe their mode of action. Furthermore, miPs have the ability to regulate proteins of diverse functions, emphasizing their value as biotechnological tools.}, language = {en}, number = {1}, urldate = {2022-11-30}, journal = {BioMolecular Concepts}, author = {Graeff, Moritz and Wenkel, Stephan}, month = feb, year = {2012}, keywords = {homotypic interaction, interfering protein, microProtein, protein-protein interaction, transcription factor inactivation}, pages = {71--78}, }
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@article{staudt_regulation_2011, title = {Regulation of protein function by ‘{microProteins}’}, volume = {12}, issn = {1469-221X}, url = {https://www.embopress.org/doi/full/10.1038/embor.2010.196}, doi = {10.1038/embor.2010.196}, abstract = {Many proteins achieve their function by acting as part of multi-protein complexes. The formation of these complexes is highly regulated and mediated through domains of protein?protein interaction. Disruption of a complex or of the ability of the proteins to form homodimers, heterodimers or multimers can have severe consequences for cellular function. In this context, the formation of dimers and multimers can be perturbed by proteins referred to here as ?microProteins?. These disruptive protein species contain the protein-interaction domains of bona fide interaction partners, but lack the functional domains required for the activation of, for example, transcription or DNA binding. MicroProteins thus behave as post-translational regulators by forming homotypic dimers with their targets, and act through the dominant?negative suppression of protein complex function. Although the first microProtein was identified more than two decades ago, the recent discovery and characterization of three further small protein species in plants emphasizes their importance. The studies discussed in this review demonstrate that the action of microProteins is general and that it has evolved in both the animal and the plant kingdoms.}, number = {1}, urldate = {2022-11-30}, journal = {EMBO reports}, author = {Staudt, Annica-Carolin and Wenkel, Stephan}, month = jan, year = {2011}, keywords = {Id-like proteins, homotypic interactions, protein–protein interaction, transcription factors}, pages = {35--42}, }
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@article{jang_arabidopsis_2008, title = {Arabidopsis {COP1} shapes the temporal pattern of {CO} accumulation conferring a photoperiodic flowering response}, volume = {27}, issn = {0261-4189}, url = {https://www.embopress.org/doi/full/10.1038/emboj.2008.68}, doi = {10.1038/emboj.2008.68}, abstract = {The transcriptional regulator CONSTANS (CO) promotes flowering of Arabidopsis under long summer days (LDs) but not under short winter days (SDs). Post-translational regulation of CO is crucial for this response by stabilizing the protein at the end of a LD, whereas promoting its degradation throughout the night under LD and SD. We show that mutations in CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1), a component of a ubiquitin ligase, cause extreme early flowering under SDs, and that this is largely dependent on CO activity. Furthermore, transcription of the CO target gene FT is increased in cop1 mutants and decreased in plants overexpressing COP1 in phloem companion cells. COP1 and CO interact in vivo and in vitro through the C-terminal region of CO. COP1 promotes CO degradation mainly in the dark, so that in cop1 mutants CO protein but not CO mRNA abundance is dramatically increased during the night. However, in the morning CO degradation occurs independently of COP1 by a phytochrome B-dependent mechanism. Thus, COP1 contributes to day length perception by reducing the abundance of CO during the night and thereby delaying flowering under SDs.}, number = {8}, urldate = {2022-11-30}, journal = {The EMBO Journal}, author = {Jang, Seonghoe and Marchal, Virginie and Panigrahi, Kishore C S and Wenkel, Stephan and Soppe, Wim and Deng, Xing-Wang and Valverde, Federico and Coupland, George}, month = apr, year = {2008}, keywords = {CONSTANS, flowering, photomorphogenesis, ubiquitin ligase}, pages = {1277--1288}, }
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@article{wenkel_feedback_2007, title = {A {Feedback} {Regulatory} {Module} {Formed} by {LITTLE} {ZIPPER} and {HD}-{ZIPIII} {Genes}}, volume = {19}, issn = {1040-4651}, url = {https://doi.org/10.1105/tpc.107.055772}, doi = {10.1105/tpc.107.055772}, abstract = {The Arabidopsis thaliana REVOLUTA (REV) protein is a member of the class III homeodomain-leucine zipper (HD-ZIPIII) proteins. REV is a potent regulator of leaf polarity and vascular development. Here, we report the identification of a gene family that encodes small leucine zipper–containing proteins (LITTLE ZIPPER [ZPR] proteins) where the leucine zipper is similar to that found in REV, PHABULOSA, and PHAVOLUTA proteins. The transcript levels of the ZPR genes increase in response to activation of a steroid-inducible REV protein. We show that the ZPR proteins interact with REV in vitro and that ZPR3 prevents DNA binding by REV in vitro. Overexpression of ZPR proteins in Arabidopsis results in phenotypes similar to those seen when HD-ZIPIII function is reduced. We propose a negative feedback model in which REV promotes transcription of the ZPR genes. The ZPR proteins in turn form heterodimers with the REV protein, preventing it from binding DNA. The HD-ZIPIII/ZPR regulatory module would serve not only to dampen the effect of fluctuations in HD-ZIPIII protein levels but more importantly would provide a potential point of regulation (control over the ratio of inactive heterodimers to active homodimers) that could be influenced by other components of the pathway governing leaf polarity.}, number = {11}, urldate = {2022-11-30}, journal = {The Plant Cell}, author = {Wenkel, Stephan and Emery, John and Hou, Bi-Huei and Evans, Matthew M.S. and Barton, M.K.}, month = nov, year = {2007}, pages = {3379--3390}, }
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@article{laubinger_arabidopsis_2006, title = {Arabidopsis {SPA} proteins regulate photoperiodic flowering and interact with the floral inducer {CONSTANS} to regulate its stability}, volume = {133}, issn = {0950-1991}, url = {https://doi.org/10.1242/dev.02481}, doi = {10.1242/dev.02481}, abstract = {The four-member SPA protein family of Arabidopsis acts in concert with the E3 ubiquitin ligase COP1 to suppress photomorphogenesis in dark-grown seedlings. Here, we demonstrate that SPA proteins are, moreover, essential for photoperiodic flowering. Mutations in SPA1 cause phyA-independent early flowering under short day (SD) but not long day (LD) conditions, and this phenotype is enhanced by additional loss of SPA3 and SPA4 function. These spa1 spa3 spa4 triple mutants flower at the same time in LD and SD, indicating that the SPA gene family is essential for the inhibition of flowering under non-inductive SD. Among the four SPA genes, SPA1 is necessary and sufficient for normal photoperiodic flowering. Early flowering of SD-grown spa mutant correlates with strongly increased FT transcript levels, whereas COtranscript levels are not altered. Epistasis analysis demonstrates that both early flowering and FT induction in spa1 mutants is fully dependent on CO. Consistent with this finding, SPA proteins interact physically with CO in vitro and in vivo, suggesting that SPA proteins regulate CO protein function. Domain mapping shows that the SPA1-CO interaction requires the CCT-domain of CO, but is independent of the B-box type Zn fingers of CO. We further show that spa1 spa3 spa4 mutants exhibit strongly increased CO protein levels, which are not caused by a change in COgene expression. Taken together, our results suggest, that SPA proteins regulate photoperiodic flowering by controlling the stability of the floral inducer CO.}, number = {16}, urldate = {2022-11-30}, journal = {Development}, author = {Laubinger, Sascha and Marchal, Virginie and Gentilhomme, José and Wenkel, Stephan and Adrian, Jessika and Jang, Seonghoe and Kulajta, Carmen and Braun, Helen and Coupland, George and Hoecker, Ute}, month = aug, year = {2006}, pages = {3213--3222}, }
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@article{wenkel_constans_2006, title = {{CONSTANS} and the {CCAAT} {Box} {Binding} {Complex} {Share} a {Functionally} {Important} {Domain} and {Interact} to {Regulate} {Flowering} of {Arabidopsis}}, volume = {18}, issn = {1040-4651}, url = {https://doi.org/10.1105/tpc.106.043299}, doi = {10.1105/tpc.106.043299}, abstract = {The CCT (for CONSTANS, CONSTANS-LIKE, TOC1) domain is found in 45 Arabidopsis thaliana proteins involved in processes such as photoperiodic flowering, light signaling, and regulation of circadian rhythms. We show that this domain exhibits similarities to yeast HEME ACTIVATOR PROTEIN2 (HAP2), which is a subunit of the HAP2/HAP3/HAP5 trimeric complex that binds to CCAAT boxes in eukaryotic promoters. Moreover, we demonstrate that CONSTANS (CO), which promotes Arabidopsis flowering, interacts with At HAP3 and At HAP5 in yeast, in vitro, and in planta. Mutations in CO that delay flowering affect residues highly conserved between CCT and the DNA binding domain of HAP2. Taken together, these data suggest that CO might replace At HAP2 in the HAP complex to form a trimeric CO/At HAP3/At HAP5 complex. Flowering was delayed by overexpression of At HAP2 or At HAP3 throughout the plant or in phloem companion cells, where CO is expressed. This phenotype was correlated with reduced abundance of FLOWERING LOCUS T (FT) mRNA and no change in CO mRNA levels. At HAP2 or At HAP3 overexpression may therefore impair formation of a CO/At HAP3/At HAP5 complex leading to reduced expression of FT. During plant evolution, the number of genes encoding HAP proteins was greatly amplified, and these proteins may have acquired novel functions, such as mediating the effect of CCT domain proteins on gene expression.}, number = {11}, urldate = {2022-11-30}, journal = {The Plant Cell}, author = {Wenkel, Stephan and Turck, Franziska and Singer, Kamy and Gissot, Lionel and Le Gourrierec, José and Samach, Alon and Coupland, George}, month = nov, year = {2006}, pages = {2971--2984}, }
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@article{becker_regulation_2003, title = {Regulation of the {ABA}-sensitive {Arabidopsis} potassium channel gene {GORK} in response to water stress}, volume = {554}, copyright = {FEBS Letters 554 (2003) 1873-3468 © 2015 Federation of European Biochemical Societies}, issn = {1873-3468}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1016/S0014-5793%2803%2901118-9}, doi = {10.1016/S0014-5793(03)01118-9}, abstract = {The phytohormone abscisic acid (ABA) regulates many stress-related processes in plants. In this context ABA mediates the responsiveness of plants to environmental stresses such as drought, cold or salt. In response to water stress, ABA induces stomatal closure by activating Ca2+, K+ and anion channels in guard cells. To understand the signalling pathways that regulate these turgor control elements, we studied the transcriptional control of the K+ release channel gene GORK that is expressed in guard cells, roots and vascular tissue. GORK transcription was up-regulated upon onset of drought, salt stress and cold. The wilting hormone ABA that integrates responses to these stimuli induced GORK expression in seedlings in a time- and concentration-dependent manner and this induction was dependent on extracellular Ca2+. ABA-responsive expression of GORK was impaired in the ABA-insensitive mutants abi1-1 and abi2-1, indicating that these protein phosphatases are regulators of GORK expression. Application of ABA to suspension-cultured cells for 2 min followed by a 4 h chase was sufficient to manifest transcriptional activation of the K+ channel gene. As predicted for a process involved in drought adaptation, only 12–24 h after the release of the stress hormone, GORK mRNA slowly decreased. In contrast to other tissues, GORK expression as well as K+ out channel activity in guard cells is ABA insensitive, allowing the plant to adjust stomatal movement and water status control separately.}, language = {en}, number = {1-2}, urldate = {2022-11-30}, journal = {FEBS Letters}, author = {Becker, D. and Hoth, S. and Ache, P. and Wenkel, S. and Roelfsema, M.r.g. and Meyerhoff, O. and Hartung, W. and Hedrich, R.}, year = {2003}, keywords = {Abscisic acid, GORK, Guard cell, K+ channel, Water stress}, pages = {119--126}, }
Vi är intresserade av att förstå hur växter använder små proteiner för att dynamiskt anpassa tillväxt och utveckling till miljöförändringar.
Det finns en växande förståelse för att proteomerna är mer komplexa än man tidigare trott. Fram till nyligen klassificerades till exempel gener som kodar för proteiner med mindre än 100 aminosyror ofta som artefakter. Detta ledde till att många av dessa små gener inte togs med i genombeskrivningarna. Förutom dessa enskilda, individuella små gener kan små proteiner också uppstå genom processer som alternativ splicing eller alternativa transkriptionella startpunkter. En gen kan alltså koda för mer än ett protein. Dessa processer gör att det finns mycket fler olika proteiner i cellen än antalet proteinkodande gener i genomet.
I vår forskning använder vi både proteincentrerade metoder (baserade på identifiering och karakterisering av specifika små proteiner, ofta mikroProteiner) och processorienterade metoder, där vi försöker förstå hur växter dynamiskt ändrar sin utveckling som respons på miljöförändringar. För att identifiera små proteiner, såsom mikroProteiner i ett sekvenserat genom, har vi utvecklat mjukvaran miPFinder, som kan klassificera små proteiner som mikroProteiner (Straub och Wenkel, 2017). Biologiska processer som vi studerar är växtens reaktion på skugga eller hur blomning initieras som en reaktion på förändrad dagslängd och temperatur. Vi har bland annat kunnat visa att små B-box-mikroProteiner påverkar när växten blommar betydligt (Graeff et al., 2016).
Vad kommer härnäst? På grund av sin ringa storlek och förmågan att förutsäga proteininteraktioner är mikroProteiner väl lämpade för reglering av bioteknologiska processer. Med hjälp av nya verktyg för genomteknik undersöker vi för närvarande möjligheten att skapa mikroProteiner de novo för att påverka växtens utveckling.