Innovation, conservation and repurposing of gene function in plant root cell type development

Abstract

Plant species have evolved myriads of solutions to adapt to dynamic environments, 35 including complex cell type development and regulation. To understand this diversity, we profiled tomato root cell type translatomes and chromatin accessibility. Using xylem differentiation in tomato, relative to Arabidopsis, examples of functional innovation, repurposing and conservation of transcription factors are described. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Translatome 40 analyses of rice, tomato and Arabidopsis tissues suggest that root meristems are more conserved, and that the functions of constitutively expressed genes are more conserved than those of cell 45 Arabidopsis inflorescence stem vascular bundles and is not expressed in primary root xylem 4 (15), and two HD-ZIPIII TFs, SlPHB/PHV (Solyc02g069830) and SlCORONA (Solyc03g120910), whose Arabidopsis orthologs regulate root protoxylem vessel differentiation via positional signals derived from a miR165/166 gradient (2,11,16). Contrary to their function in Arabidopsis, over-expression of SlbZIP11 or SlKNAT1 was sufficient to specify additional protoxylem cell files ( Fig. 2C-D), although these files were often non-contiguous for the 5 SlbZIP11 lines (Fig. 2C) (statistical analyses in Fig. S5, Data S3). The bHLH and MYB overexpression lines had no vascular phenotype. Relative to Arabidopsis, In the case of SlKNAT1, this demonstrates "repurposed" regulation, while in the case of SlbZIP11 it represents innovation in function. miRNA-resistant versions of SlCORONA and SlPHB/PHV were sufficient to regulate protoxylem vessel identity and patterning within the vascular cylinder 10 similar to their Arabidopsis function and are thus conserved regulators (Fig. 2D, E).Cell type/tissue translatomes are likely dynamic over developmental time and in response to the environment. In Arabidopsis, cell type-enriched genes that maintain expression despite stress are also critical regulators of cell fate (3, 17). However, the majority of plant cell type profiles are 15

Acis-regulatory atlas in maize at single-cell resolution

“…Maintaining focus on PCC development, we aligned Z. mays and A. thaliana trajectories using a time-warping algorithm. Consistent with recent comparative analysis of vascular development in O. sativa , A. thaliana, and Solanum lycopersicum 38 , only 206 out of 10,976 putative orthologs were significantly associated (FDR < 0.01) with PCC pseudotime in both species, indicating that the majority PCC trajectories-associated genes are unique to each lineage (97% Z. mays , 83% A. thaliana ). However, of the 206 PCC-associated orthologs, ∼50% (102/206) exhibited similar patterns of gene accessibility across pseudotime ( Fig.…”

Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation

“…Notably, MYB86, which has previously been associated with lignification during xylem formation ( Patzlaff et al, 2003 ), functions as a hub at both 3 and 5 DAGs. Gene clusters that are downstream of MYB86 are associated with xylem formation, including numerous peroxidase genes, NAC-related TF genes, and HOMEOBOX LEUCINE ZIPPER-14 ( HAT14 ; Marjamaa et al, 2009 ; Kajala et al, 2020 ). We predicted additional hubs at 5 DAGs, including LBD4 (CA02g00820) and LBD25 (CA02g30000).…”

Convergent evolution of gene regulatory networks underlying plant adaptations to dry environments

“…It is possible that the sporadic appearance of exodermis during plant evolution was possible through rewiring regulatory networks of Casparian strips and suberin lamellae formation in endodermis or similar lignin and suberin biosynthetic pathways from other cell types. The coexistence of endodermis and exodermis in roots has complicated transcriptomic approaches, and to investigate the exodermis gene expression and GRNs in individual species, methods such as laser capture microdissection (LCM) and translating ribosome affinity purification (TRAP) have been used (Kajala et al, 2021;. The exodermis-specific gene expression patterns and GRNs are a foundation for understanding the genetic underpinnings of the cell type and enable investigating its evolutionary paths.…”

“…Recent studies are showing the importance of distinct clades of the MYB transcription factor family as conserved regulators of suberin deposition in response to osmotic stress in different cell types and in phylogenetically distant plants, linking their evolution with colonization of dry terrestrial environments by early land plants (Capote et al, 2018;Cohen, Fedyuk, Wang, Wu, & Aharoni, 2020;Gou et al, 2017;Kajala et al, 2021;Kosma et al, 2014;Lashbrooke et al, 2016;Legay et al, 2016;Shukla et al, 2021;To et al, 2020;Wei et al, 2020). Two of the possible scenarios are: (1) osmotic stress-inducible regulation of suberization diversified from pre-existing developmental pathways, (2) the regulation of suberization in response to drought was re-activated as plants colonized drier environments.…”

“…Its plasticity may have involved the co-option of regulatory genes from the endodermis, and may have convergently occurred in some flowering plant lineages (Angiosperms) submitted to constant environmental water fluctuations (Figure 1) (Perumalla, Peterson, & Enstone, 1990). Due to the coexistence of endodermis and exodermis in roots, separation of these cell types for gene expression analyses has been required to understand which genes and GRNs are active in each cell type, and to assess co-option and innovation in exodermis GRN evolution (Kajala et al, 2021;.…”