VASCULAR DEVELOPMENT IN PERENNIAL PLANTS AND ITS PLASTICITY TO COPE WITH ABIOTIC STRESSES

Group Leader: Daniel Conde Rodríguez - Junior Lider de la Caixa
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Personnel:

 

Orcid: 0000-0001-8362-4190
Scopus: 55455766600  

 
Overview


The secondary xylem, or wood, is the most abundant natural product on earth. Wood is a product of the activity of a secondary meristem, the vascular cambium. Differentiation of secondary xylem cells requires spatial distribution of molecular signals that vary in accord with the position of the specific cell type. Forward genetic and functional genomics approaches have identified genes affecting secondary xylem formation. However, the characterization of the molecular signals and genes that determine the specific cell fate for a tracheary element, a fiber, or a parenchymatic cell remains elusive.


Research lines

1. Decoding the signals that trigger xylem cell types from vascular cambial cells

Uncovering the mechanisms that determine the intricated cellular organization of the secondary xylem has been elusive, partly due to the technical difficulties of exploring such a small population of cells and their differentiation from the vascular cambium stem cells. We have previously used single-nuclei RNA sequencing (snRNA-seq) to determine cell type-specific transcriptomes of the Populus vegetative shoot apex. Motivated by the high similarities between Populus and Arabidopsis cell populations in the vegetative apex, we applied a pipeline for interspecific single-cell data integration. We contrasted the developmental trajectories of primary phloem and xylem formation in both species, establishing the first comparison of vascular development between a model annual herbaceous and a woody perennial plant species. We will apply snRNA-seq to infer the developmental trajectories from vascular cambium to secondary xylem cells and identify the regulators of each cell type differentiation. To verify the role of these putative regulators, genetic perturbation of candidates will be carried out, and their effect on vascular development will be assessed.



Figure 1. Characterization of the cell-type specific transcriptomes at the Populus vegetative shoot apex.



Figure 2. Comparison between the developmental programs of the primary vasculature formation of Populus and Arabidopsis.



Figure 3. Validation of cell type identity by promoter::GUS fusions


2. Identification of the molecular basis of the poplar vascular development modifications to cope with drought

The plasticity of wood anatomy development in response to abiotic stresses such as drought is an adaptative mechanism that allows poplar trees to better adapt to water availability with unwanted side effects. Understanding the mechanisms of wood anatomy and plant hydraulics plasticity is critical for developing genetically improved germplasm that better adapts to climate shifts, allowing for greater resilience, enhancing their productivity, and reducing the cost of biomass production and its environmental impact. Our objective is to identify molecular mechanisms that promote wood developmental changes in response to drought in poplar by applying recently developed technologies to dissect heterogeneous cell populations and characterize the transcriptomes of individual cells.




Figure 4. Trees respond to drought with a diverse tissue-specific mechanism including wood anatomical changes that confer drought resistance. We will apply single-cell transcriptomics to uncover the regulatory genes for the wood developmental changes under drought.



3. Soil phytoremediation of heavy metal pollutants by genetically enhanced trees in combination with mutualistic microorganisms

This research aims to implement a phytoremediation strategy for soils contaminated with heavy metals. To develop this strategy, the chosen plant species is poplar (Populus tremula X alba). The project is divided into three specific objectives:

1. Generation and selection of genetically improved poplar lines for their accumulation capacity and tolerance to heavy metals.
2. Selection of mutualistic microorganisms isolated from areas contaminated with heavy metals.
3. Toxicity tests and accumulation of heavy metals assays in genetically improved poplar lines in combination with selected mutualistic microorganisms.




Figure 5. Heavy metals toxicity assays in poplar wild type trees.


Funding

  • Identifying the molecular regulatory mechanisms of stem cell differentiation during the formation of new organs in trees, by applying single-cell transcriptomics to Daniel Conde. 2023-2026. La Caixa Junior Leader Fellowship Incoming.




  • MoReGrow: Molecular bases of poplar response to environmental cues and abiotic stresses for maximizing plant growth to Mariano Perales. 2022-2025. Proyectos I+D+i -Modalidades «Retos Investigación» y «Generación de Conocimiento». Proyecto PID2021-123060OB-I00 financiado por MCIN/ AEI /10.13039/501100011033/ y por FEDER Una manera de hacer Europa.

 

  • BIOSYSMO: Bioremediation Systems Exploiting Synergies for Improved Removal of Mixed Pollutants to Isabel Allona. 2022-2026. Funded by the European Union under the GA no 101060211.


 

 


Representative Publications

Sreedasyam, A., Plott, C., Hossain, M.S., Lovell, J.T., Grimwood, J., Jenkins, J.W., Daum, C., Barry, K., Carlson, J., Shu, S., Phillips, J., Amirebrahimi, M., Zane, M., Wang, M., Goodstein, D., Haas, F.B., Hiss, M., Perroud, P.-F., Jawdy, S.S., Yang, Y., Hu, R., Johnson, J., Kropat, J., Gallaher, S.D., Lipzen, A., Shakirov, E.V., Weng, X., Torres-Jerez, I., Weers, B., Conde, D., Pappas, M.R., Liu, L., Muchlinski, A., Jiang, H., Shyu, C., Huang, P., Sebastian, J., Laiben, C., Medlin, A., Carey, S., Carrell, A.A., Chen, J.-G., Perales, M., Swaminathan, K., Allona, I., Grattapaglia, D., Cooper, E.A., Tholl, D., Vogel, J.P., Weston, D.J., Yang, X., Brutnell, T.P., Kellogg, E.A., Baxter, I., Udvardi, M., Tang, Y., Mockler, T.C., Juenger, T.E., Mullet, J., Rensing, S.A., Tuskan, G.A., Merchant, S.S., Stacey, G., Schmutz, J. 2023. JGI Plant Gene Atlas: an updateable transcriptome resource to improve functional gene descriptions across the plant kingdom. Nucleic Acids Research 51, 8383–8401. DOI: 10.1093/nar/gkad616

Vigneaud, J., Kohler, A., Sow, M.D., Delaunay, A., Fauchery, L., Guinet, F., Daviaud, C., Barry, K.W., Keymanesh, K., Johnson, J., Singan, V., Grigoriev, I., Fichot, R., Conde, D., Perales, M., Tost, J., Martin, F.M., Allona, I., Strauss, S.H., Veneault-Fourrey, C., Maury, S. 2023. DNA hypomethylation of the host tree impairs interaction with mutualistic ectomycorrhizal fungus. New Phytologist. DOI: 10.1111/nph.18734

Conde, D., Kirst, M. 2022. Decoding exceptional plant traits by comparative single-cell genomics. Trends in Plant Science 27, 1095–1098. DOI: 10.1016/j.tplants.2022.08.006

Conde, D., Triozzi, P.M., Pereira, W.J., Schmidt, H.W., Balmant, K.M., Knaack, S.A., Redondo-López, A., Roy, S., Dervinis, C., Kirst, M. 2022. Single-nuclei transcriptome analysis of the shoot apex vascular system differentiation in Populus. Development 149, dev200632. DOI: 10.1242/dev.200632

Vigneaud, J., Kohler, A., Sow, M.D., Delaunay, A., Fauchery, L., Guinet, F., Daviaud, C., Barry, K.W., Keymanesh, K., Johnson, J., Singan, V., Grigoriev, I., Fichot, R., Conde, D., Perales, M., Tost, J., Martin, F.M., Allona, I., Strauss, S.H., Veneault-Fourrey, C., Maury, S. n.d. DNA hypomethylation of the host tree impairs interaction with mutualistic ectomycorrhizal fungus. New Phytologist n/a. DOI: 10.1111/nph.18734

Knaack, S.A., Conde, D., Chakraborty, S., Balmant, K.M., Irving, T.B., Maia, L.G.S., Triozzi, P.M., Dervinis, C., Pereira, W.J., Maeda, J., Schmidt, H.W., Ané, J.-M., Kirst, M., Roy, S. 2022. Temporal change in chromatin accessibility predicts regulators of nodulation in Medicago truncatula. BMC Biology 20, 252. DOI: 10.1186/s12915-022-01450-9

Irving, T.B., Chakraborty, S., Maia, L.G.S., Knaack, S., Conde, D., Schmidt, H.W., Triozzi, P.M., Simmons, C.H., Roy, S., Kirst, M., Ané, J.-M. 2022. An LCO-responsive homolog of NODULE INCEPTION positively regulates lateral root formation in Populus sp.. Plant Physiology 190, 1699–1714. DOI: 10.1093/plphys/kiac356

Pereira, W.J., Knaack, S., Chakraborty, S., Conde, D., Folk, R.A., Triozzi, P.M., Balmant, K.M., Dervinis, C., Schmidt, H.W., Ané, J.-M., Roy, S., Kirst, M. 2022. Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen-fixing clade. New Phytologist 234, 634–649. DOI: 10.1111/nph.18006

Triozzi, P.M., Irving, T.B., Schmidt, H.W., Keyser, Z.P., Chakraborty, S., Balmant, K., Pereira, W.J., Dervinis, C., Mysore, K.S., Wen, J., Ané, J.-M., Kirst, M., Conde, D. 2022. Spatiotemporal cytokinin response imaging and ISOPENTENYLTRANSFERASE 3 function in Medicago nodule development. Plant Physiology 188, 560–575. DOI: 10.1093/plphys/kiab447

Pereira, W.J., Almeida, F.M., Conde, D., Balmant, K.M., Triozzi, P.M., Schmidt, H.W., Dervinis, C., Pappas, G.J., Kirst, M. 2021. Asc-Seurat: analytical single-cell Seurat-based web application. BMC Bioinformatics 22, 556. DOI: 10.1186/s12859-021-04472-2

Triozzi, P.M., Schmidt, H.W., Dervinis, C., Kirst, M., Conde, D. 2021. Simple, efficient and open-source CRISPR/Cas9 strategy for multi-site genome editing in Populus tremula × alba. Tree Physiology 41, 2216–2227. DOI: 10.1093/treephys/tpab066

Conde, D., Triozzi, P.M., Balmant, K.M., Doty, A.L., Miranda, M., Boullosa, A., Schmidt, H.W., Pereira, W.J., Dervinis, C., Kirst, M. 2021. A robust method of nuclei isolation for single-cell RNA sequencing of solid tissues from the plant genus Populus. PLOS ONE 16, e0251149. DOI: 10.1371/journal.pone.0251149

Gómez-Soto, D., Ramos-Sánchez, J.M., Alique, D., Conde, D., Triozzi, P.M., Perales, M., Allona, I. 2021. Overexpression of a SOC1-Related Gene Promotes Bud Break in Ecodormant Poplars. Frontiers in Plant Science 12.

Balmant, K.M., Noble, J.D., Alves, F.C., Dervinis, C., Conde, D., Schmidt, H.W., Vazquez, A.I., Barbazuk, W.B., Campos, G. de los, Resende, M.F.R., Kirst, M. 2020. Xylem systems genetics analysis reveals a key regulator of lignin biosynthesis in Populus deltoides. Genome Research 30, 1131–1143. DOI: 10.1101/gr.261438.120

Ribeiro, C.L., Conde, D., Balmant, K.M., Dervinis, C., Johnson, M.G., McGrath, A.P., Szewczyk, P., Unda, F., Finegan, C.A., Schmidt, H.W., Miles, B., Drost, D.R., Novaes, E., Gonzalez-Benecke, C.A., Peter, G.F., Burleigh, J.G., Martin, T.A., Mansfield, S.D., Chang, G., Wickett, N.J., Kirst, M. 2020. The uncharacterized gene EVE contributes to vessel element dimensions in Populus. Proceedings of the National Academy of Sciences 117, 5059–5066. DOI: 10.1073/pnas.1912434117

Conde, D., Perales, M., Sreedasyam, A., Tuskan, G.A., Lloret, A., Badenes, M.L., González-Melendi, P., Ríos, G., Allona, I. 2019. Engineering Tree Seasonal Cycles of Growth Through Chromatin Modification. Frontiers in Plant Science 10.

Ramos-Sánchez, J.M., Triozzi, P.M., Moreno-Cortés, A., Conde, D., Perales, M., Allona, I. 2017. Real-time monitoring of PtaHMGB activity in poplar transactivation assays. Plant Methods 13, 50. DOI: 10.1186/s13007-017-0199-x

Conde, D., Moreno-Cortés, A., Dervinis, C., Ramos-Sánchez, J.M., Kirst, M., Perales, M., González-Melendi, P., Allona, I. 2017. Overexpression of DEMETER, a DNA demethylase, promotes early apical bud maturation in poplar. Plant, Cell & Environment 40, 2806–2819. DOI: 10.1111/pce.13056

Conde, D., Le Gac, A.-L., Perales, M., Dervinis, C., Kirst, M., Maury, S., González-Melendi, P., Allona, I. 2017. Chilling-responsive DEMETER-LIKE DNA demethylase mediates in poplar bud break. Plant, Cell & Environment 40, 2236–2249. DOI: 10.1111/pce.13019

Conde, D., González-Melendi, P., Allona, I. 2013. Poplar stems show opposite epigenetic patterns during winter dormancy and vegetative growth. Trees 27, 311–320. DOI: 10.1007/s00468-012-0800-x