Innovation, conservation, and repurposing of gene function in 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:10.1016/j.cell.2021.04.024

Cited by 60 publications

(66 citation statements)

References 129 publications

(175 reference statements)

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“…These robust crops could grow better in salinized or dry soil with fewer nutrients which will help to close the yield gap in the future and reduce the use of freshwater resources. The recent emergence of molecular technologies including single-cell sequencing, CRISPR/CAS9 genome editing as well as tissue- and cell-specific promoters studies for imaging of cellular processes will greatly contribute to our understanding of crop root plasticity under stress ( Shulse et al, 2019 ; Kajala et al, 2021 ; Lyzenga et al, 2021 ).…”

Section: Discussion and Perspectivesmentioning

confidence: 99%

Root plasticity under abiotic stress

et al. 2021

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Abiotic stresses increasingly threaten existing ecological and agricultural systems across the globe. Plant roots perceive these stresses in the soil and adapt their architecture accordingly. This review provides insights into recent discoveries showing the importance of root system architecture and plasticity for the survival and development of plants under heat, cold, drought, salt, and flooding stress. In addition, we review the molecular regulation and hormonal pathways involved in controlling root system architecture plasticity, main root growth, branching and lateral root growth, root hair development and formation of adventitious roots. Several stresses affect root anatomy by causing aerenchyma formation, lignin and suberin deposition, and Casparian strip modulation. Roots can also actively grow towards favourable soil conditions and avoid environments detrimental to their development. Recent advances in understanding the cellular mechanisms behind these different root tropisms are discussed. Understanding root plasticity will be instrumental for the development of crops that are resilient in the face of abiotic stress.

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Section: Discussion and Perspectivesmentioning

confidence: 99%

Root plasticity under abiotic stress

et al. 2021

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“…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 and translating ribosome affinity purification (TRAP) have been used (Kajala et al, 2021 ; Shiono et al, 2014 ). 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.…”

Section: Root Cell Type Grn Adaptations To Drought: Impermeabilization Of Endodermis and Exodermismentioning

confidence: 99%

“…Recent studies are showing the importance of distinct clades of the MYB TF 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 et al, 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: (a) osmotic stress–inducible regulation of suberization diversified from pre‐existing developmental pathways and (b) the regulation of suberization in response to drought was re‐activated as plants colonized drier environments.…”

Section: Root Cell Type Grn Adaptations To Drought: Impermeabilization Of Endodermis and Exodermismentioning

confidence: 99%

“…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 et al, 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 ; Shiono et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

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

Artur

Kajala

2021

Plant Cell & Environment

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Plants transitioned from an aquatic to a terrestrial lifestyle during their evolution. On land, fluctuations on water availability in the environment became one of the major problems they encountered. The appearance of morpho‐physiological adaptations to cope with and tolerate water loss from the cells was undeniably useful to survive on dry land. Some of these adaptations, such as carbon concentrating mechanisms (CCMs), desiccation tolerance (DT) and root impermeabilization, appeared in multiple plant lineages. Despite being crucial for evolution on land, it has been unclear how these adaptations convergently evolved in the various plant lineages. Recent advances on whole genome and transcriptome sequencing are revealing that co‐option of genes and gene regulatory networks (GRNs) is a common feature underlying the convergent evolution of these adaptations. In this review, we address how the study of CCMs and DT has provided insight into convergent evolution of GRNs underlying plant adaptation to dry environments, and how these insights could be applied to currently emerging understanding of evolution of root impermeabilization through different barrier cell types. We discuss examples of co‐option, conservation and innovation of genes and GRNs at the cell, tissue and organ levels revealed by recent phylogenomic (comparative genomic) and comparative transcriptomic studies.

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“…A recent comparative translatome analysis [21] shows that, across plant species, mechanisms regulating meristematic cell activity are better conserved than those characterizing other cell populations. This supports our observations regarding the similarity of VC behaviour along the root-stem axis.…”

Section: Introductionmentioning

confidence: 99%

Meristematic Connectome: A Cellular Coordinator of Plant Responses to Environmental Signals?

Chiatante

Montagnoli

Trupiano

et al. 2021

Cells

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Mechanical stress in tree roots induces the production of reaction wood (RW) and the formation of new branch roots, both functioning to avoid anchorage failure and limb damage. The vascular cambium (VC) is the factor responsible for the onset of these responses as shown by their occurrence when all primary tissues and the root tips are removed. The data presented confirm that the VC is able to evaluate both the direction and magnitude of the mechanical forces experienced before coordinating the most fitting responses along the root axis whenever and wherever these are necessary. The coordination of these responses requires intense crosstalk between meristematic cells of the VC which may be very distant from the place where the mechanical stress is first detected. Signaling could be facilitated through plasmodesmata between meristematic cells. The mechanism of RW production also seems to be well conserved in the stem and this fact suggests that the VC could behave as a single structure spread along the plant body axis as a means to control the relationship between the plant and its environment. The observation that there are numerous morphological and functional similarities between different meristems and that some important regulatory mechanisms of meristem activity, such as homeostasis, are common to several meristems, supports the hypothesis that not only the VC but all apical, primary and secondary meristems present in the plant body behave as a single interconnected structure. We propose to name this structure “meristematic connectome” given the possibility that the sequence of meristems from root apex to shoot apex could represent a pluricellular network that facilitates long-distance signaling in the plant body. The possibility that the “meristematic connectome” could act as a single structure active in adjusting the plant body to its surrounding environment throughout the life of a plant is now proposed.

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

Cited by 60 publications

References 129 publications

Root plasticity under abiotic stress

Root plasticity under abiotic stress

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

Meristematic Connectome: A Cellular Coordinator of Plant Responses to Environmental Signals?

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