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The dynamic and diverse nature of parenchyma cells in the Arabidopsis root during secondary growth

ABSTRACT: During secondary growth, the vascular cambium produces conductive xylem and phloem cells, while the phellogen (cork cambium) deposits phellem (cork) as the outermost protective barrier. Although most of the secondary tissues are made up by parenchyma cells which are also produced by both cambia, their diversity and function are poorly understood. Here we combined single-cell RNA sequencing analysis with lineage tracing to recreate developmental trajectories of the cell types in the Arabidopsis root undergoing secondary growth. By analysing 93 reporter lines, we were able to identify 20 different cell types or cell states, many of which have not been described before. We additionally observed distinct transcriptome signatures of parenchyma cells depending on their maturation state and proximity to the conductive cell types. Our data shows that both xylem and phloem parenchyma tissues are required for normal formation of conductive tissue cell types. Furthermore, we showed that mature phloem parenchyma gradually obtains periderm identity, and this transformation can be accelerated by jasmonate (JA) or wounding. Thus, our study reveals the diversity of parenchyma cells and their capacity to undergo considerable identity changes during the secondary growth.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE270140 | GEO | 2025/01/14

REPOSITORIES: GEO

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Project description:The phellogen or cork cambium is a bifacial stem cell population from which derivatives are formed by periclinal divisions and specified on opposing sides as phelloderm (inwardly) and phellem or cork (outwardly). Altogether the three layers constitute the periderm which covers and protects the radially-grown organs (stems, roots and tubers) and wounded tissues from dehydration and pathogen attack. The phellem is the final responsible of the protective function of periderm and despite its vital importance, just the suberin biosynthetic process has been studied molecularly while other processes are poorly understood. To shed some light on the phellem cell development from its formation to its final maturation, we used the innercork living material of cork planks extracted from cork oak (Quercus suber) in which we analysed the transcriptome at three time-points: at the beginning (April), maximum (June) and final (July) cork seasonal growth. Since cork presents seasonal growth and the process from phellogen derivative proliferation and specification to phellem cells is continuous, the time-course cork samples were used to approach the phellem cell formation and development. The June enrichment of phellem cells undergoing suberization was confirmed transcriptionally, observing highest expression of suberin-related genes in this month, thus validating our strategy. To highlight the major molecular processes embracing from phellogen to mature phellem cell, the differentially expressed genes between time-points were clustered based on their expression pattern. April transcriptome upregulates the processes involved in the meristem proliferation and maintenance and the triggering of cell differentiation, in agreement with the enrichment of phellogenic cells from which phellem cells are specified. The processes upregulated in Juny and July cork samples, were secondary metabolic processes compatible with the biosynthesis of secondary metabolites deposited within phellem cell wall such as suberin, lignin, extractives including fatty aciyl-derived compounds and triterpenes and also soluble aromatic compounds. The processes with a maximum in July showed upregulation of polyssacharides- and lignin-related processes compatible with a reinforcement of the cork cell wall, presumably related with the latecork formation with smaller and thickened-cells at the end of the growing season. For the above mentioned processes, we discuss the putative function of the most relevant genes in the context of phellem ontogeny. This work provides the most important molecular mechanisms during phellem cell development and provide relevant data for the understanding of the seasonal growth of cork, a material of important circular economic value.

Project description:Vascular cambium is a secondary meristem which produces xylem (wood) inwards and phloem (bark) outwards. The activity of cambium leads to expansion in the diameters in plants, that is, secondary growth, and thus contributes to biomass increase. The regulation of cambium development is at multilevel including phytohormones and peptide-receptor kinase (CLE41/44-PXY) signalling pathways. However, only limited progress has been made on the transcriptional regulation level. To construct the transcriptional network that regulates cambium development, we performed a genome wide transcript profiling in sorted procambial and cambial cells in Arabidopsis roots. More than 500 genes were identified as cambium abundant genes via comparison against transcriptomes of other Arabidopsis root cell types. We then investigated the roles of almost all the cambial transcription factors (TFs) and some of their homologous genes during secondary growth. Many of the candidate TFs were highly expressed in cambium based on the promoter GUS fusion and in situ hybridization. An unbiased transcriptional regulatory network was constructed using transcript profiling data collected from inducible overexpression lines for selected candidate TFs and a few major nodes were identified in the network including WOX4 and KNAT1. Moreover, the severity of mutant phenotypes was predicted based on the network. Next, we used the predication as a guide and generated over 70 double mutants within the same or among different TF families to explore the genetic interactions of candidate genes. Phenotype characterization on the secondary growth of the mutants and the overexpression lines identified promoters and inhibitors of cambium activity. The phenotypic data also suggested the redundancy within and among TF families because the phenotypes could be enhanced when additional TFs were mutated. We also found that combinations of certain overexpression lines and mutants led to pronounced increase of cell proliferation or xylem differentiation and in the extreme case the formation of ectopic cambium. We herein propose that cambium development is orchestrated by a wide network at the transcriptional level, where each TF has a different contribution to cell proliferation and differentiation.

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The dynamic and diverse nature of parenchyma cells in the Arabidopsis root during secondary growth

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