Regulation of DELLA proteins by post-translational modifications

[EN] DELLA proteins are the negative regulators of the gibberellin (GA) signaling pathway. GAs have a pervasive effect on plant physiology, influencing processes that span the entire life cycle of the plant. All the information encoded by GAs, either environmental or developmental in origin, is canalized through DELLAs, which modulate the activity of many transcription factors and transcriptional regulators. GAs unlock the signaling pathway by triggering DELLA polyubiquitination and degradation by the 26S proteasome. Recent reports indicate, however, that there are other pathways that trigger DELLA polyubiquitination and degradation independently of GAs. Moreover, results gathered during recent years indicate that other post-translational modifications (PTMs), namely phosphorylation, SUMOylation and glycosylation, modulate DELLA function. The convergence of several PTMs in DELLA therefore highlights the strict regulation to which these proteins are subject. In this review, we summarize these discoveries and discuss DELLA PTMs from an evolutionary perspective and examine the possibilities these and other post-translational regulations offer to improve DELLA-dependent agronomic traits.The Spanish Ministry of Science and Innovation (PID2019-109925GB-I00 to D.A.) and the European Union (H2020-MSCA-IF-2016-746396 to A.S.-M.). We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).Blanco-Touriñán, N.; Serrano-Mislata, A.; Alabadí Diego, D. (2020). Regulation of DELLA proteins by post-translational modifications. Plant and Cell Physiology. 61(11):1891-1901. https://doi.org/10.1093/pcp/pcaa113S18911901611

Differential growth at the apical hook: all roads lead to auxin

[EN] The apical hook is a developmentally regulated structure that appears in dicotyledonous seedlings when seeds germinate buried in the soil. It protects the shoot apical meristem and cotyledons from damage while the seedling is pushing upwards seeking for light, and it is formed by differential cell expansion between both sides of the upper part of the hypocotyl. Its apparent simplicity and the fact that it is dispensable when seedlings are grown in vitro have converted the apical hook in one of the favorite experimental models to study the regulation of differential growth. The involvement of hormones especially auxin in this process was manifested already in the early studies. Remarkably, a gradient of this hormone across the hook curvature is instrumental to complete its development, similar to what has been proposed for other processes involving the bending of an organ, such as tropic responses. In agreement with this, other hormones-mainly gibberellins and ethylene-and the light, regulate in a timely and interconnected manner the auxin gradient to promote hook development and its opening, respectively. Here, we review the latest findings obtained mainly with the apical hook of Arabidopsis thaliana, paying special attention to the molecular mechanisms for the cross-regulation between the different hormone signaling pathways that underlie this developmental process.This work was supported by grants from the Spanish Ministry of Science and Innovation (BIO2010-15071 and CSD2007-00057) and the Generalitat Valenciana (ACOMP/2011/288 and PROMETEO/2010/020).Abbas, M.; Alabadí Diego, D.; Blazquez Rodriguez, MA. (2013). Differential growth at the apical hook: all roads lead to auxin. Frontiers in Plant Science. 4:441-1-441-9. https://doi.org/10.3389/fpls.2013.00441S441-1441-9

Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis

[EN] Plasticity and robustness of signaling pathways partly rely on genetic redundancy, although the precise mechanism that provides functional specificity to the different redundant elements in a given process is often unknown. In Arabidopsis, functional redundancy in gibberellin signaling has been largely attributed to the presence of five members of the DELLA family of transcriptional regulators. Here, we demonstrate that two evolutionarily and functionally divergent DELLA proteins, RGL2 and RGA, can perform exchangeable functions when they are expressed under control of the reciprocal promoter. Furthermore, both DELLA proteins display equivalent abilities to interact with PIF4 and with other bHLH transcription factors with a reported role in the control of cell growth and seed germination. Therefore, we propose that functional diversification of Arabidopsis DELLA proteins has largely relied on changes in their gene expression patterns rather than on their ability to interact with different regulatory partners, model also supported by a clustering analysis of DELLA transcript profiles over a range of organs and growth conditions that revealed specific patterns of expression for each of these genes.We deeply appreciate the help of Marta Trenor and Laura Garcia-Carcel in the initial stages of this work. We also thank Tai-ping Sun (Duke University) and the Arabidpsis Biological Resource Center for seeds, Marta Boter for the pGBKT7 and pGADT7 Gateway vectors, Santiago Elena (IBMCP, CSIC-UPV) for useful comments on the manuscript, and Francois Parcy (IRTSV, CNRS-CEA) for fruitful discussions and hosting MAB. Work in the authors' laboratories is funded by grants BIO2007-60923 and BIO2005-07284 from the Spanish Ministry of Science and Innovation. J.G.B. is the recipient of a CSIC I3P Fellowship and J.A.M. is the recipient of a Fellowship from the Fundacion "la Caixa.Gallego-Bartolome, J.; Minguet, E.; Marin, JA.; Prat, S.; Blazquez Rodriguez, MA.; Alabadí Diego, D. (2010). Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Molecular Biology and Evolution. 27(6):1247-1256. https://doi.org/10.1093/molbev/msq0121247125627

Induction of auxin biosynthesis and WOX5 repression mediate changes in root development in Arabidopsis exposed to chitosan

[EN] Chitosan is a natural polymer with applications in agriculture, which causes plasma membrane permeabilisation and induction of intracellular reactive oxygen species (ROS) in plants. Chitosan has been mostly applied in the phylloplane to control plant diseases and to enhance plant defences, but has also been considered for controlling root pests. However, the effect of chitosan on roots is virtually unknown. In this work, we show that chitosan interfered with auxin homeostasis in Arabidopsis roots, promoting a 2-3 fold accumulation of indole acetic acid (IAA). We observed chitosan dose-dependent alterations of auxin synthesis, transport and signalling in Arabidopsis roots. As a consequence, high doses of chitosan reduce WOX5 expression in the root apical meristem and arrest root growth. Chitosan also propitiates accumulation of salicylic (SA) and jasmonic (JA) acids in Arabidopsis roots by induction of genes involved in their biosynthesis and signalling. In addition, high-dose chitosan irrigation of tomato and barley plants also arrests root development. Tomato root apices treated with chitosan showed isodiametric cells respect to rectangular cells in the controls. We found that chitosan causes strong alterations in root cell morphology. Our results highlight the importance of considering chitosan dose during agronomical applications to the rhizosphere.This work was supported by AGL 2015 66833-R Grant from the Spanish Ministry of Economy and Competitiveness Grant AGL 2015. We would like to thank Drs Isabel Lopez-Diaz and Esther Carrera for plant hormone quantitation (IBMCP, Valencia, Spain). Part of this work was filed for a patent (P201431399) by L. V. Lopez-Llorca, F. Lopez-Moya and N. Escudero as inventors. We would like to thank Dr Michael Kershaw (University of Exeter) for his English revision and critical comments of the manuscript. 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Hormonal regulation of temperature-induced growth in Arabidopsis

[EN] Successful plant survival depends upon the proper integration of information from the environment with endogenous cues to regulate growth and development. We have investigated the interplay between ambient temperature and hormone action during the regulation of hypocotyl elongation, and we have found that gibberellins (GAs) and auxin are quickly and independently recruited by temperature to modulate growth rate, whereas activity of brassinosteroids (BRs) seems to be required later on. Impairment of GA biosynthesis blocked the increased elongation caused at higher temperatures, but hypocotyls of pentuple DELLA knockout mutants still reduced their response to higher temperatures when BR synthesis or auxin polar transport were blocked. The expression of several key genes involved in the biosynthesis of GAs and auxin was regulated by temperature, which indirectly resulted in coherent variations in the levels of accumulation of nuclear GFP-RGA (repressor of GA1) and in the activity of the DR5 reporter. DNA microarray and genetic analyses allowed the identification of the transcription factor PIF4 (phytochrome-interacting factor 4) as a major target in the promotion of growth at higher temperature. These results suggest that temperature regulates hypocotyl growth by individually impinging on several elements of a pre-existing network of signaling pathways involving auxin, BRs, GAs, and PIF4.We thank G. Choi (KAIST, Daejeon, South Korea), C. Fankhauser (University of Lausanne, Lausanne, Switzerland), T. Guilfoyle (Department of Biochemistry, University of Missouri, MO, USA), N. P. Harberd (Department of Plant Sciences, University of Oxford, Oxford, UK), E. Huq (University of Texas, Austin, TX, USA), T-p Sun (Department of Biology, Duke University, Durham, USA), S. G. Thomas (Rothamsted Research, Hertfordshire, UK), G. Vert (Institut de Biologie Integrative des Plantes, Montpellier, France), Z. Y. Wang (Department of Plant Biology, Carnegie Institution, Stanford, USA), Y. Yin (Plant Science Institute, Iowa State University, Ames, IA, USA), and the Arabidopsis Biological Resource Center for seeds; and X. W. Deng (Yale University, New Haven, CT, USA) for antibodies against RPT5. We also thank Dr Jorge Casal (Universidad de Buenos Aires, Buenos Aires, Argentina) for helpful suggestions on this work. Work in the authors' laboratories is funded by grant BIO2007-60923 from the Spanish Ministry of Science and Innovation and by grant 167890/110 from the Norwegian Research Council. JG-B was supported by a JAE pre-doctoral fellowship from CSIC.Stavang, JA.; Gallego-Bartolomé, J.; Gómez Jiménez, MD.; Yoshida, S.; Asami, T.; Olsen, JE.; García-Martínez, JL.... (2009). Hormonal regulation of temperature-induced growth in Arabidopsis. The Plant Journal. 60(4):589-601. https://doi.org/10.1111/j.1365-313X.2009.03983.x58960160

Long-Day Photoperiod Enhances Jasmonic Acid-Related Plant Defense

[EN] Agricultural crops are exposed to a range of daylengths, which act as important environmental cues for the control of developmental processes such as flowering. To explore the additional effects of daylength on plant function, we investigated the transcriptome of Arabidopsis (Arabidopsis thaliana) plants grown under short days (SD) and transferred to long days (LD). Compared with that under SD, the LD transcriptome was enriched in genes involved in jasmonic acid-dependent systemic resistance. Many of these genes exhibited impaired expression induction under LD in the phytochrome A (phyA), cryptochrome 1 (cry1), and cry2 triple photoreceptor mutant. Compared with that under SD, LD enhanced plant resistance to the necrotrophic fungus Bottytis cinerea. This response was reduced in the phyA cry1 cry2 triple mutant, in the constitutive photomorphogenicl (cop1) mutant, in the myc2 mutant, and in mutants impaired in DELLA function. Plants grown under SD had an increased nuclear abundance of COP1 and decreased DELLA abundance, the latter of which was dependent on COP1. We conclude that growth under LD enhances plant defense by reducing COP1 activity and enhancing DELLA abundance and MYC2 expression.This study was supported by a Guggenheim Foundation fellowship (to J.J.C), by Agencia Nacional de Promocion Cientifica y Tecnologica (PICT-2015-1796), by the University of Buenos Aires (20020100100437, to J.J.C.), by the Howard Hughes Medical Institute (J.I.C.), and by the SIGNAT-Research and Innovation Staff Exchange (H2020-MSCA-RISE-2014, to P.D.C., M.A.B., D.A., and J.J.C.).Cagnola, J.; Cerdan, P.; Pacín, M.; Andrade, A.; Rodríguez, V.; Zurbriggen, M.; Legris, M.... (2018). Long-Day Photoperiod Enhances Jasmonic Acid-Related Plant Defense. PLANT PHYSIOLOGY. 178(1):163-173. https://doi.org/10.1104/pp.18.00443S163173178

A genetic approach reveals different modes of action of prefoldins

[EN] The prefoldin complex (PFDc) was identified in humans as a co-chaperone of the cytosolic chaperonin T-COMPLEX PROTEIN RING COMPLEX (TRiC)/CHAPERONIN CONTAINING TCP-1 (CCT). PFDc is conserved in eukaryotes and is composed of subunits PFD1-6, and PFDc-TRiC/CCT folds actin and tubulins. PFDs also participate in a wide range of cellular processes, both in the cytoplasm and in the nucleus, and their malfunction causes developmental alterations and disease in animals and altered growth and environmental responses in yeast and plants. Genetic analyses in yeast indicate that not all of their functions require the canonical complex. The lack of systematic genetic analyses in plants and animals, however, makes it difficult to discern whether PFDs participate in a process as the canonical complex or in alternative configurations, which is necessary to understand their mode of action. To tackle this question, and on the premise that the canonical complex cannot be formed if one subunit is missing, we generated an Arabidopsis (Arabidopsis thaliana) mutant deficient in the six PFDs and compared various growth and environmental responses with those of the individual mutants. In this way, we demonstrate that the PFDc is required for seed germination, to delay flowering, or to respond to high salt stress or low temperature, whereas at least two PFDs redundantly attenuate the response to osmotic stress. A coexpression analysis of differentially expressed genes in the sextuple mutant identified several transcription factors, including ABA INSENSITIVE 5 (ABI5) and PHYTOCHROME-INTERACTING FACTOR 4, acting downstream of PFDs. Furthermore, the transcriptomic analysis allowed assigning additional roles for PFDs, for instance, in response to higher temperature.This work was supported by grants from the Spanish Ministry of Economy and Competitiveness and "Agencia Estatal de Investigacion"/FEDER/European Union (BIO2013-43184-P to D.A. and M.A.B., and BIO2016-79133-P and PID2019-109925GB-I00 to D.A.). N.B.-T., A.S.-M., and A.P.-A. were recipient of Ministerio de Economia y Competitividad (BES-2014-068868), EU MSCA-IF (H2020-MSCA-IF-2016746396) and Ministerio de Educacion (FPU17/05186) fellowships, respectively.Esteve-Bruna, D.; Blanco-Touriñán, N.; Serrano-Mislata, A.; Esquinas-Ariza, RM.; Resentini, F.; Forment Millet, JJ.; Carrasco-López, C.... (2021). A genetic approach reveals different modes of action of prefoldins. Plant Physiology. 187(3):1534-1550. https://doi.org/10.1093/plphys/kiab348S15341550187

Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins

[EN] The ability of plants to provide a plastic response to environmental cues relies on the connectivity between signaling pathways. DELLA proteins act as hubs that relay environmental information to the multiple transcriptional circuits that control growth and development through physical interaction with transcription factors from different families. We have analyzed the presence of one DELLA protein at the Arabidopsis genome by chromatin immunoprecipitation coupled to large-scale sequencing and we find that it binds at the promoters of multiple genes. Enrichment analysis shows a strong preference for cis elements recognized by specific transcription factor families. In particular, we demonstrate that DELLA proteins are recruited by type-B ARABIDOPSIS RESPONSE REGULATORS (ARR) to the promoters of cytokinin-regulated genes, where they act as transcriptional co-activators. The biological relevance of this mechanism is underpinned by the necessity of simultaneous presence of DELLAs and ARRs to restrict root meristem growth and to promote photomorphogenesis.This work was funded by grants BIO2007-60923 and BIO2010-15071 from the Spanish Ministry of Economy and Innovation (MAB); grant ERC-2011-StG_20101109 from the European Research Council (JUL); grants BB/J/00426X/1 and BB/E022618/1 from the Biotechnology and Biological Sciences Research Council (SGT); the Professorial Research Fellowship award BB/G023972/1 from the Biotechnology and Biological Sciences Research Council (KH and MJB); and grant FP7-311929 from the European Union (RPB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Marín-De La Rosa, NA.; Pfeiffer, A.; Hill, K.; Locascio ., AAM.; Bhalerao, R.; Miskolczi, P.; Grønlund, A.... (2015). Genome Wide Binding Site Analysis Reveals Transcriptional Coactivation of Cytokinin-Responsive Genes by DELLA Proteins. PLoS Genetics. 11(7):1-20. https://doi.org/10.1371/journal.pgen.100533712011

The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and transcription start site determination in Arabidopsis

Eukaryotes have evolved multiple ATP-dependent chromatin remodelers to shape the nucleosome landscape. We recently uncovered an evolutionarily conserved SWItch/Sucrose Non-Fermentable (SWI/SNF) chromatin remodeler complex in plants reminiscent of the mammalian BAF subclass, which specifically incorporates the MINUSCULE (MINU) catalytic subunits and the TRIPLE PHD FINGERS (TPF) signature subunits. Here we report experimental evidence that establishes the functional relevance of TPF proteins for the complex activity. Our results show that depletion of TPF triggers similar pleiotropic phenotypes and molecular defects to those found in minu mutants. Moreover, we report the genomic location of MINU2 and TPF proteins as representative members of this SWI/SNF complex and their impact on nucleosome positioning and transcription. These analyses unravel the binding of the complex to thousands of genes where it modulates the position of the +1 nucleosome. These targets tend to produce 5′-shifted transcripts in the tpf and minu mutants pointing to the participation of the complex in alternative transcription start site usage. Interestingly, there is a remarkable correlation between +1 nucleosome shift and 5′ transcript length change suggesting their functional connection. In summary, this study unravels the function of a plant SWI/SNF complex involved in +1 nucleosome positioning and transcription start site determination.MCIN/AEI/10.13039/501100011033 [RYC2018-024108-I, PID2019-108577GA-I00 to J.G.B.]. Funding for open access charge: CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI)

AUXIN BINDING PROTEIN1 links cell wall remodelling, auxin signalling and cell expansion in Arabidopsis

[EN] Cell expansion is an increase in cell size and thus plays an essential role in plant growth and development. Phytohormones and the primary plant cell wall play major roles in the complex process of cell expansion. In shoot tissues, cell expansion requires the auxin receptor AUXIN BINDING PROTEIN1 (ABP1), but the mechanism by which ABP1 affects expansion remains unknown. We analyzed the effect of functional inactivation of ABP1 on transcriptomic changes in dark-grown hypocotyls and investigated the consequences of gene expression on cell wall composition and cell expansion. Molecular and genetic evidence indicates that ABP1 affects the expression of a broad range of cell wall-related genes, especially cell wall remodeling genes, mainly via an SCFTIR/AFB-dependent pathway. ABP1 also functions in the modulation of hemicellulose xyloglucan structure. Furthermore, fucosidase-mediated defucosylation of xyloglucan, but not biosynthesis of nonfucosylated xyloglucan, rescued dark-grown hypocotyl lengthening of ABP1 knockdown seedlings. In muro remodeling of xyloglucan side chains via an ABP1-dependent pathway appears to be of critical importance for temporal and spatial control of cell expansion.We thank Markus Pauly (University of California, Berkeley) for kindly providing the seeds of AXY8 overexpressor, Mark Estelle (University of California, San Diego, Howard Hughes Medical Institute) for seeds of the triple tir afb2 afb3 mutant, Xing Wang Deng (Yale University) for seeds of cop10-4, Doan Luu (CNRS, Montpellier) for seeds of the 35S: PIP2; 1-GFP line, and Jiri Friml (Institute of Science and Technology, Vienna) for seeds of the abp1-5 mutant. We thank Sylvie Citerne from the Plant Observatory at Institut Jean-Pierre Bourgin (INRA) for cell wall composition analysis. This work has benefitted from the facilities and expertise of the Imagif Cell Biology Unit of the Gif campus, which is supported by the Conseil General de l'Essonne, France. We also thank Jessica Marion for technical assistance in electron microscopy. This work was supported by the ANR blanc AuxiWall Project ANR-11-BSV5-0007. C.P.-R.'s team is also funded by the CNRS and G.M. by INRA. Work in the laboratories of D.A. and M.A.B. was supported by grants from the Spanish Ministry of Science and Innovation (BIO2010-15071 and CSD2007-00057) and the Generalitat Valenciana (ACOMP/2011/288 and PROMETEO/2010/020). We thank Philip Harris (University of Auckland) and Spencer Brown (Institut des Sciences du Vegetal, CNRS) for critical reading of the article and useful comments.Parque, S.; Mouille, G.; Grandont, L.; Alabadí Diego, D.; Gaertner, C.; Goyallon, A.; Muller, P.... (2014). AUXIN BINDING PROTEIN1 links cell wall remodelling, auxin signalling and cell expansion in Arabidopsis. Plant Cell. 26(1):280-291. https://doi.org/10.1105/tpc.113.120048S28029126