A functionally informed evolutionary framework for the study of LRR-RLKs during stem cell maintenance

Cammarata, Joseph; Scanlon, Michael J.

doi:10.1007/s10265-020-01197-w

Cited by 10 publications

(6 citation statements)

References 49 publications

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“…In contrast to flowering plants, Physcomitrium encodes only three orthologs of stem cell-regulating LRR-RLKs. This relative simplicity makes moss an appealing model for understanding the role of these receptors in stem cell specification 15 . We previously characterized the function of CLV1 and RPK2 orthologs in Physcomitrium and found that these genes performed similar developmental functions in moss and moss 16 , including regulation of SAM homeostasis.…”

Section: Introductionmentioning

confidence: 99%

Cytokinin-CLAVATA crosstalk is an ancient mechanism regulating shoot meristem homeostasis in land plants

Cammarata

Farfan

Scanlon

et al. 2021

Preprint

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Plant shoots grow from stem cells within Shoot Apical Meristems (SAMs), which produce lateral organs while maintaining the stem cell pool. In the model flowering plant Arabidopsis, the CLAVATA (CLV) pathway functions antagonistically with cytokinin signaling to control the size of the multicellular SAM via negative regulation of the stem cell organizer WUSCHEL (WUS). Although comprising just a single cell, the SAM of the model moss Physcomitrium patens (formerly Physcomitrella) performs equivalent functions during stem cell maintenance and organogenesis, despite the absence of WUS-mediated stem cell organization. Our previous work showed that the stem cell-delimiting function of the CLV pathway receptors CLAVATA1 (CLV1) and RECEPTOR-LIKE PROTEIN KINASE2 (RPK2) is conserved in the moss P. patens. Here, we use P. patens to assess whether CLV-cytokinin crosstalk is also an evolutionarily conserved feature of stem cell regulation. Genetic analyses reveal that CLV1 and RPK2 regulate SAM proliferation via separate pathways in moss. Surprisingly, cytokinin receptor mutants also form ectopic stem cells in the absence of cytokinin signaling. Through modeling, we identified regulatory network archtectures that recapitulated the stem cell phenotypes of clv1 and rpk2 mutants, cytokinin application, cytokinin receptor mutations, and higher-order combinations of these perturbations. These models predict that CLV1 and RPK2 act through separate pathways wherein CLV1 represses cytokinin-mediated stem cell initiation and RPK2 inhibits this process via a separate, cytokinin-independent pathway. Our analysis suggests that crosstalk between CLV1 and cytokinin signaling is an evolutionarily conserved feature of SAM homeostasis that preceded the role of WUS in stem cell organization.

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Section: Introductionmentioning

confidence: 99%

Cytokinin-CLAVATA crosstalk is an ancient mechanism regulating shoot meristem homeostasis in land plants

Cammarata

Farfan

Scanlon

et al. 2021

Preprint

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“…An approach similar to what we have shown here with the integration of phylogenetic, functional and structural information, should facilitate the disentanglement of distinct evolutionary histories of peptide ligands and their receptors in mono- and dicots. One study along these lines have recently been published on the BAM/CLV1/TDR receptors and CLE peptides (Cammarata and Scanlon, 2020).…”

Section: Introductionmentioning

confidence: 99%

The Sequenced Genomes of Non-Flowering Land Plants Reveal the (R)Evolutionary History of Peptide Signaling

Furumizu¹,

Krabberød

Hammerstad

et al. 2020

Preprint

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An understanding of land plant evolution is a prerequisite for in-depth knowledge of plant biology. Here we illustrate how to extract and explore information hidden in the increasing number of sequenced plant genomes, from bryophytes to angiosperms, to elucidate a specific biological question – how peptide signaling evolved. To conquer land and cope with changing environmental conditions, plants have gone through profound transformations that must have required a revolution in cell-to-cell communication. Peptides can act as signals of endogenous and exogenous changes, and interactions with leucine-rich repeat receptor-like kinases activate intracellular molecular signaling. Signaling peptides are typically active in organs like flowers and seeds, vascular tissue, root and shoot meristems, which are absent in the most primitive land plants. However, putative orthologues for several peptide-receptor pairs have been identified in non-seed land plants. These discoveries and elucidation of co-evolution of such ligands and their receptors, have profound implications for the understanding of evolution and diversity of cell-to-cell communication, as de novo interactions in peptide signaling pathways may have contributed to generate novel traits in land plants. Phylogenetic analyses, genomic, structural and functional data can guide us to reveal evolutionary steps that laid the foundation for a wealth of diversified terrestrial plants.

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“…In contrast to flowering plants, the moss Physcomitrium patens (previously known as Physcomitrella patens ) encodes only three orthologs of stem cell–regulating LRR-RLKs: PpCLV1a , PpCLV1b , and PpRPK2 . This relative simplicity makes P. patens an appealing model for understanding the role of these receptors in stem cell specification ( 15 ). We previously characterized the function of CLV1 and RPK2 orthologs in P. patens and found that these genes performed similar developmental functions in flowering plants and P. patens ( 16 ), including regulation of SAM homeostasis.…”

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confidence: 99%

Cytokinin–CLAVATA cross-talk is an ancient mechanism regulating shoot meristem homeostasis in land plants

Cammarata

Farfan

Scanlon

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Significance Plants grow from their tips. The gametophore (shoot-like organ) tip of the moss Physcomitrium patens is a single cell that performs the same functions as those of multicellular flowering plants, producing the cells that make leaves and regenerating new stem cells to maintain the shoot tip. Several pathways, including CLAVATA and cytokinin hormonal signaling, regulate stem cell abundance in flowering plants and in mosses, although the mechanisms whereby these pathways regulate stem cell abundance and their conservation between these plant lineages is poorly understood. Using moss, we investigated how Pp CLAVATA and cytokinin signaling interact. Overall, we found evidence that Pp CLAVATA and cytokinin signaling interact similarly in moss and flowering plants, despite their distinct anatomies, life cycles, and evolutionary distance.

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A functionally informed evolutionary framework for the study of LRR-RLKs during stem cell maintenance

Cited by 10 publications

References 49 publications

Cytokinin-CLAVATA crosstalk is an ancient mechanism regulating shoot meristem homeostasis in land plants

Cytokinin-CLAVATA crosstalk is an ancient mechanism regulating shoot meristem homeostasis in land plants

The Sequenced Genomes of Non-Flowering Land Plants Reveal the (R)Evolutionary History of Peptide Signaling

Cytokinin–CLAVATA cross-talk is an ancient mechanism regulating shoot meristem homeostasis in land plants

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