Innovation, Conservation and Repurposing of Gene Function in Plant Root Cell Type Development

Kajala, Kaisa; Gouran, Mona; Shaar-Moshe, Lidor; Mason, G. Alex; Rodriguez‐Medina, Joel; Kawa, Dorota; Pauluzzi, Germain; Reynoso, Mauricio; Cantó-Pastor, Alex; Manzano, Concepción; Lau, Vincent; Artur, Mariana A S; West, Donnelly A.; Gray, Sharon B.; Borowsky, Alexander T.; Moore, Bryshal P.; Yao, Andrew I.; Morimoto, Kevin W.; Bajic, Marko; Formentin, Elide; Nirmal, Niba; Rodriguez, Alan; Pasha, Asher; Deal, Roger B.; Kliebenstein, Daniel J.; Hvidsten, Torgeir R.; Provart, Nicholas J.; Sinha, Neelima; Runcie, Daniel E.; Bailey‐Serres, Julia; Brady, Siobhán M.

doi:10.2139/ssrn.3733189

Cited by 4 publications

(4 citation statements)

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“…To explore the degree of regulatory conservation in angiosperm root development, we profiled chromatin accessibility in 4,655 nuclei from 7-day old embryonic root tissues in the eudicot model species A. thaliana, integrated with previously generated A. thaliana root scRNAseq data (n=12,606), and constructed eight cis-regulatory pseudotime trajectories encompassing vascular, dermal and ground development (Figure7A-7C, S11 and S12A; TableS13-S17).Maintaining focus on PCC development, we first validated the utility of the integrated data sets by visualizing gene expression and accessibility of known marker genes representative of QC (WUSCHEL-RELATED HOMEOBOX 5, WOX5), procambial (WUSCHEL-RELATED HOMEOBOX 4, WOX4) and PCC (SUCROSE TRANSPORTER 2, SUC2) cell types (Figure7Dand 7E). Next, we aligned Z. mays and A. thaliana PCC trajectories using a time-warping algorithm to enable direct comparison of gene accessibility dynamics in a common space.Consistent with recent comparative analysis of vascular development in O. sativa, A. thaliana, and Solanum lycopersicum(Kajala et al, 2020), 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 (Figure 7F, 7G, S12B).…”

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confidence: 85%

Acis-regulatory atlas in maize at single-cell resolution

Marand

Chen

Gallavotti

et al. 2020

Preprint

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Cis-regulatory elements (CREs) encode the genomic blueprints for coordinating spatiotemporal gene expression programs underlying highly specialized cell functions. To identify CREs underlying cell-type specification and developmental transitions, we implemented single-cell sequencing of Assay for Transposase Accessible Chromatin in an atlas of Zea mays organs. We describe 92 distinct states of chromatin accessibility across more than 165,913 putative CREs, 56,575 cells, and 52 known cell-types in maize using a novel implementation of regularized quasibinomial logistic regression. Cell states were largely determined by combinatorial accessibility of transcription factors (TFs) and their binding sites. A neural network revealed that cell identity could be accurately predicted (>0.94) solely based on TF binding site accessibility. Co-accessible chromatin recapitulated higher-order chromatin interactions, with distinct sets of TFs coordinating cell type-specific regulatory dynamics. Pseudotime reconstruction and alignment with Arabidopsis thaliana trajectories identified conserved TFs, associated motifs, and cis-regulatory regions specifying sequential developmental progressions. Cell-type specific accessible chromatin regions were enriched with phenotype-associated genetic variants and signatures of selection, revealing the major cell-types and putative CREs targeted by modern maize breeding. Collectively, our analysis affords a comprehensive framework for understanding cellular heterogeneity, evolution, and cis-regulatory grammar of cell-type specification in a major crop species.

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confidence: 85%

Acis-regulatory atlas in maize at single-cell resolution

Marand

Chen

Gallavotti

et al. 2020

Preprint

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“…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 DAG. Gene clusters that are downstream of MYB86 are associated with xylem formation, including numerous peroxidase genes, NAC-related TFs, and HOMEOBOX LEUCINE ZIPPER-14 (HD-ZIP 14) (Kajala et al, 2020; Marjamaa et al, 2009). We predicted additional hubs 5 DAG, including LBD4 (CA02g00820) and LBD25 (CA02g30000), which were recently implicated in the related process of haustorium formation during plant parasitism (Jhu et al, 2021; Melnyk, 2017).…”

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confidence: 99%

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

Thomas

Broeck

Spurney

et al. 2021

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Graft incompatibility is a poorly understood phenomenon that presents a serious agricultural challenge. Unlike immediate incompatibility that results in rapid death, delayed incompatibility can take months or even years to manifest, creating a significant economic burden for perennial crop production. To gain insight into the genetic mechanisms underlying this phenomenon, we developed a model system with Solanum lycopersicum 'tomato' and Capsicum annuum 'pepper' heterografting, which expresses signs of anatomical junction failure within the first week of grafting. By generating a detailed timeline for junction formation we were able to pinpoint the cellular basis for this delayed incompatibility. Furthermore, we infer gene regulatory networks for compatible self-grafts versus incompatible heterografts based on these key anatomical events, which predict core regulators for grafting. Finally, we delve into the role of vascular development in graft formation and validate SlWOX4 as a regulator for grafting in tomato. Notably, SlWOX4 is the first gene to be functionally implicated in vegetable crop grafting.

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“…It is possible that the 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. 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, 2020;Kosma et al, 2014;Lashbrooke et al, 2016;Legay et al, 2016;To et al, 2020;Wei et al, 2020). Two of the possible scenarios are: (1) osmotic stress-inducible regulation of suberization diversified from preexisting developmental pathways, (2) the regulation of suberization in response to drought was re-activated as plants colonized drier environments.…”

Section: Cell Type Adaptation To Drought: Root Endodermis and Exodermismentioning

confidence: 99%

An evolutionary perspective of plant adaptations to dry environments

Artur

Kajala

2020

Preprint

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Plants transitioned from an aquatic to a terrestrial lifestyle during their evolution. On land, drought became one of the major problems they encountered, as it impacts correct cell functioning necessary to support life. The evolution of morphophysiological and molecular adaptations to cope with and tolerate drough was undeniably useful to survive on land. Some of these adaptations appeared repeatedly in phylogenetically distant species, showing a signature of convergent evolution. Details of this convergent evolution are now being assessed thanks to recent developments on high throughput phenotyping and whole genome and transcriptome sequencing. Phylogenomic (comparative genomic) and comparative transcriptomic analyses are revealing complex, well-coordinated and intricate gain and loss of genes and co-option of gene regulatory networks underlying cell and tissue specific adaptations to moderate and extreme drought in phylogenetically distant species. Here we review recent research on signatures of convergent evolution of regulatory networks underlying carbon concentrating mechanisms such as C4 and CAM photosynthesis, desiccation tolerance in seeds and resurrection plants, and impermeabilization of root exodermis.

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Innovation, Conservation and Repurposing of Gene Function in Plant Root Cell Type Development

Cited by 4 publications

References 0 publications

Acis-regulatory atlas in maize at single-cell resolution

Acis-regulatory atlas in maize at single-cell resolution

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

An evolutionary perspective of plant adaptations to dry environments

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