期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：14
DOI：10.1073/pnas.2116860119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：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
PpCLAVATA and cytokinin signaling interact. Overall, we found evidence that
PpCLAVATA and cytokinin signaling interact similarly in moss and flowering plants, despite their distinct anatomies, life cycles, and evolutionary distance.
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 patens) 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 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 cross-talk is also an evolutionarily conserved feature of stem cell regulation. Application of cytokinin produces ectopic stem cell phenotypes similar to
Ppclv1a,
Ppclv1b, and
Pprpk2 mutants. Surprisingly, cytokinin receptor mutants also form ectopic stem cells in the absence of cytokinin signaling. Through modeling, we identified regulatory network architectures that recapitulated the stem cell phenotypes of
Ppclv1a,
Ppclv1b, and
Pprpk2 mutants, cytokinin application, cytokinin receptor mutations, and higher-order combinations of these perturbations. These models predict that
PpCLV1 and
PpRPK2 act through separate pathways wherein
PpCLV1 represses cytokinin-mediated stem cell initiation, and
PpRPK2 inhibits this process via a separate, cytokinin-independent pathway. Our analysis suggests that cross-talk between CLV1 and cytokinin signaling is an evolutionarily conserved feature of SAM homeostasis that preceded the role of WUS in stem cell organization.
