Plant vascular development: mechanisms and environmental regulation

[EN] Plant vascular development is a complex process culminating in the generation of xylem and phloem, the plant transporting conduits. Xylem and phloem arise from specialized stem cells collectively termed (pro)cambium. Once developed, xylem transports mainly water and mineral nutrients and phloem transports photoassimilates and signaling molecules. In the past few years, major advances have been made to characterize the molecular, genetic and physiological aspects that govern vascular development. However, less is known about how the environment re-shapes the process, which molecular mechanisms link environmental inputs with developmental outputs, which gene regulatory networks facilitate the genetic adaptation of vascular development to environmental niches, or how the first vascular cells appeared as an evolutionary innovation. In this review, we (1) summarize the current knowledge of the mechanisms involved in vascular development, focusing on the model species Arabidopsis thaliana, (2) describe the anatomical effect of specific environmental factors on the process, (3) speculate about the main entry points through which the molecular mechanisms controlling of the process might be altered by specific environmental factors, and (4) discuss future research which could identify the genetic factors underlying phenotypic plasticity of vascular development.Work in the authors' laboratories is supported by funds from the Spanish Ministry of Science and Universities (BIO2016-79147-R to JA, and BFU2016-80621-P to MAB). JA holds a Ramon y Cajal contract (RYC-2014-15752). We are deeply grateful to Debra Westall (Universitat Politecnica de Valencia) for revising the manuscript. Due to space limitations, not all relevant publications could be included in this review.Agustí, J.; Blazquez Rodriguez, MA. (2020). 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ACAULIS5 Is Required for Cytokinin Accumulation and Function During Secondary Growth of Populus Trees

[EN] In the primary root and young hypocotyl of Arabidopsis, ACAULIS5 promotes translation of SUPPRESSOR OF ACAULIS51 (SAC51) and thereby inhibits cytokinin biosynthesis and vascular cell division. In this study, the relationships between ACAULIS5, SAC51 and cytokinin biosynthesis were investigated during secondary growth of Populus stems. Overexpression of ACAULIS5 from the constitutive 35S promoter in hybrid aspen (Populus tremula x Populus tremuloides) trees suppressed the expression level of ACAULIS5, which resulted in low levels of the physiologically active cytokinin bases as well as their direct riboside precursors in the transgenic lines. Low ACAULIS5 expression and low cytokinin levels of the transgenic trees coincided with low cambial activity of the stem. ACAULIS5 therefore, contrary to its function in young seedlings in Arabidopsis, stimulates cytokinin accumulation and cambial activity during secondary growth of the stem. This function is not derived from maturing secondary xylem tissues as transgenic suppression of ACAULIS5 levels in these tissues did not influence secondary growth. Interestingly, evidence was obtained for increased activity of the anticlinal division of the cambial initials under conditions of low ACAULIS5 expression and low cytokinin accumulation. We propose that ACAULIS5 integrates auxin and cytokinin signaling to promote extensive secondary growth of tree stems.This research was supported by the Swedish Research Council Formas (grant no. 232-2009-1698), the Swedish Research Council VR (grant no. 621-2013-4949), Vinnova (grant no. 201600504), Knut and Alice Wallenberg Foundation (grant no. 2016-0341), Fundacao para a Ciencia e Tecnologia (FCT), through CEEC/IND/00175/2017 contract to AM, FCT R&D Unit grants to GREEN-IT -Bioresources for Sustainability (grant no. UIDB/04551/2020), BioISI (grants nos. UIDB/04046/2020 and UIDP/04046/2020), the Spanish Ministry of Economy and Innovation (grant no. BFU2016-80621-P), and the Ministry of Education, Youth and Sports, Czech Republic through the European Regional Development Fund-Project "Plants as a Tool for Sustainable Global Development" (grant no. CZ.02.1.01/0.0/0.0/16_019/0000827).Milhinhos, A.; Bollhoner, B.; Blazquez Rodriguez, MA.; Novak, O.; Miguel, CM.; Tuominen, H. (2020). ACAULIS5 Is Required for Cytokinin Accumulation and Function During Secondary Growth of Populus Trees. Frontiers in Plant Science. 11:1-11. https://doi.org/10.3389/fpls.2020.601858S11111Agusti, J., Herold, S., Schwarz, M., Sanchez, P., Ljung, K., Dun, E. A., … Greb, T. (2011). Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. 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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

The role of a class III gibberellin 2-oxidase in tomato internode elongation

[EN] A network of environmental inputs and internal signaling controls plant growth, development and organ elongation. In particular, the growth-promoting hormone gibberellin (GA) has been shown to play a significant role in organ elongation. The use of tomato as a model organism to study elongation presents an opportunity to study the genetic control of internode-specific elongation in a eudicot species with a sympodial growth habit and substantial internodes that can and do respond to external stimuli. To investigate internode elongation, a mutant with an elongated hypocotyl and internodes but wild-type petioles was identified through a forward genetic screen. In addition to stem-specific elongation, this mutant, named tomato internode elongated -1 (tie-1) is more sensitive to the GA biosynthetic inhibitor paclobutrazol and has altered levels of intermediate and bioactive GAs compared with wild-type plants. The mutation responsible for the internode elongation phenotype was mapped to GA2oxidase 7, a class III GA 2-oxidase in the GA biosynthetic pathway, through a bulked segregant analysis and bioinformatic pipeline, and confirmed by transgenic complementation. Furthermore, bacterially expressed recombinant TIE protein was shown to have bona fide GA 2-oxidase activity. These results define a critical role for this gene in internode elongation and are significant because they further the understanding of the role of GA biosynthetic genes in organ-specific elongation.This work used the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 Instrumentation Grants S10RR029668 and S10RR027303. We thank the Tomato Genetics Resource Center for providing seed of the M82 and Heinz cultivars. The material was developed by and/or obtained from the UC Davis/C M Rick Tomato Genetics Resource Center and maintained by the Department of Plant Sciences, University of California, Davis, CA 95616, USA. We thank Anthony Bolger, Alisdair Fernie and Bjorn Usadel for providing us with access to pre-publication genomic reads of the S. lycopersicum cultivar M82, and Cristina Urbez and Noel Blanco-Tourinan (IBMCP, Spain) for technical help with in vitro production of TIE1. This work was supported in part by the Elsie Taylor Stocking Memorial Fellowship awarded to ASL in 2013, by NSF grant IOS-0820854, by USDA National Institute of Food and Agriculture project CA-D-PLB-2465-H, by internal UC Davis funds, and by Spanish Ministry of Economy and Competitiveness grant BFU2016-80621-P.Lavelle, A.; Gath, N.; Devisetty, U.; Carrera Bergua, E.; Lopez Diaz, I.; Blazquez Rodriguez, MA.; Maloof, J. (2018). The role of a class III gibberellin 2-oxidase in tomato internode elongation. 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Extremophilic bacteria restrict the growth of Macrophomina phaseolina by combined secretion of polyamines and lytic enzymes

[EN] Extremophilic microorganisms were screened as biocontrol agents against two strains of Macrophomina phaseolina (Mp02 and 06). Stenotrophomonas sp. AG3 and Exiguobacterium sp. S58 exhibited a potential in vitro antifungal effect on Mp02 growth, corresponding to 52.2% and 40.7% inhibition, respectively. This effect was confirmed by scanning electron microscopy, where images revealed marked morphological alterations in fungus hyphae. The bacteria were found to secrete lytic enzymes and polyamines. Exiguobacterium sp. S56a was the only strain able to reduce the growth of the two strains of M. phaseolina through their supernatant. Antifungal supernatant activity was correlated with the ability of bacteria to synthesize and excrete putrescine, and the exogenous application of this polyamine to the medium phenocopied the bacterial antifungal effects. We propose that the combined secretion of putrescine, spermidine, and lytic enzymes by extremophilic microorganism predispose these microorganisms to reduce the disease severity occasioned by M. phaseolina in soybean seedlings.The authors acknowledge the generous financial support by the PICT V Bicentenario 2010 1788 Project (FONCyT, Argentina). This work was performed in the context of a project called ¿Análisis de Adaptación al Cambio Climático en Humedales Andinos¿. ID: 6188775¿8-LP13. Ministerio del Medio Ambiente, Región de Antofagasta. We are also grateful to Lic. C. Pérez Brandan for providing us with the M. phaseolina strains used in this study.Santos, AP.; Nieva Muratore, L.; Sole-Gil, A.; Farías, ME.; Ferrando Monleón, AR.; Blazquez Rodriguez, MA.; Belfiore, C. (2021). Extremophilic bacteria restrict the growth of Macrophomina phaseolina by combined secretion of polyamines and lytic enzymes. Plant Biotechnology Reports. 32:1-9. https://doi.org/10.1016/j.btre.2021.e00674S193

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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Coordination between growth and stress responses by DELLA in the liverwort Marchantia polymorpha

Plant survival depends on the optimal use of resources under variable environmental conditions. Among the mechanisms that mediate the balance between growth, differentiation, and stress responses, the regulation of transcriptional activity by DELLA proteins stands out. In angiosperms, DELLA accumulation promotes defense against biotic and abiotic stress and represses cell division and expansion, while the loss of DELLA function is associated with increased plant size and sensitivity toward stress.1 Given that DELLA protein stability is dependent on gibberellin (GA) levels2 and GA metabolism is influenced by the environment,3 this pathway is proposed to relay environmental information to the transcriptional programs that regulate growth and stress responses in angiosperms.4,5 However, DELLA genes are also found in bryophytes, whereas canonical GA receptors have been identified only in vascular plants.6, 7, 8, 9, 10 Thus, it is not clear whether these regulatory functions of DELLA predated or emerged with typical GA signaling. Here, we show that, as in vascular plants, the only DELLA in the liverwort Marchantia polymorpha also participates in the regulation of growth and key developmental processes and promotes oxidative stress tolerance. Moreover, part of these effects is likely caused by the conserved physical interaction with the MpPIF transcription factor. Therefore, we suggest that the role in the coordination of growth and stress responses was already encoded in the DELLA protein of the common ancestor of land plants, and the importance of this function is underscored by its conservation over the past 450 million years

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