PpRPK2 modulates auxin homeostasis and transport to specify stem cell identity and plant shape in the moss Physcomitrella

Abstract

Plant shape is determined by the activity of stem cells in the growing tips, and evolutionary changes in shape are linked to changes in stem cell function. The CLAVATA pathway is a key regulator of stem cell function in the multicellular shoot tips of Arabidopsis, acting via the WUSCHEL transcription factor to modulate hormone homeostasis. Broad scale evolutionary comparisons have shown that CLAVATA is a conserved regulator of land plant stem cell function, but CLAVATA acts independently of WUSCHEL-like (WOX) proteins in bryophytes, raising questions about the evolution of stem cell function and the role of the CLAVATA pathway. Here we show that the moss (Physcomitrella) CLAVATA pathway affects stem cell activity and overall plant shape by modulating hormone homeostasis. CLAVATA pathway components are expressed in the tip cells of filamentous tissues, regulating cell identity, filament branching patterns and plant spread. The PpRPK2 receptor-like kinase plays the major role and is expressed more strongly than other receptor-encoding genes. Pprpk2 mutants have abnormal responses to cytokinin, and auxin transport inhibition and show reduced PIN auxin transporter expression. We propose a model whereby PpRPK2 modulates PIN activity to determine stem cell identity and overall plant form in Physcomitrella. Our data indicate that CLAVATA-mediated auxin homeostasis is a fundamental property of plant stem cell function likely exhibited by the last shared common ancestor of land plants.

Calpain DEK1 acts as a developmental switch gatekeeping cell fate transitions

“…The second order regulatory context of CLV1b (Figs 4c and SF10k) suggests that all positional and developmental queues discussed above are co-regulated in one DEK1-controlled CLAVATA regulon . Consistent with the findings from two recent studies (Nemec Venza et al, 2021; Cammarata et al, 2021), our data suggests that this DEK1-controlled, cytokinin-mediated pathway governs stem-cell homeostasis acting separately from the cytokinin-independent pathway involving the RECEPTOR-LIKE PROTEIN KINASE2 (RPK2; subnetwork VIII).…”

Leaf Morphogenesis: Insights From the Moss Physcomitrium patens

“…Specification of the shoot initial cell requires both cytokinin and auxin (Ashton et al, 1978;Cove et al, 2006;Bennett et al, 2014). Factors including DEFECTIVE KERNEL 1 (DEK1), NO GAMETOPHORES 1 and 2 (NOG1 and 2) RECEPTOR-LIKE PROTEIN KINASE 2 (RPK2), and CLAVATA (CLV) function through APETALA2-type (AP2type) transcription factors to control the frequency of shoot initial cells (Aoyama et al, 2012;Perroud et al, 2014;Moody et al, 2018Moody et al, , 2021Whitewoods et al, 2018;Demko et al, 2021;Nemec Venza et al, 2021). In P. patens, a shoot initial cell undergoes several rounds of stereotypic, oblique cell divisions that lead to the formation of a tetrahedral shoot apical cell, marking the transition from a so-called 2D to 3D growth mode (Figure 2A; Harrison et al, 2009).…”

“…In P. patens, a shoot initial cell undergoes several rounds of stereotypic, oblique cell divisions that lead to the formation of a tetrahedral shoot apical cell, marking the transition from a so-called 2D to 3D growth mode (Figure 2A; Harrison et al, 2009). These divisions are also regulated by DEK1, CLV, NOG1, and NOG2 genes (Perroud et al, 2014;Moody et al, 2018Moody et al, , 2021Whitewoods et al, 2018;Nemec Venza et al, 2021), and precisely fulfilled by mitotic spindle orientation regulators, including microtubule-associated protein TARGETING FACTOR FOR Xklp2 and SABRE (Kosetsu et al, 2017;Kozgunova et al, 2020;Cheng and Bezanilla, 2021). Additionally, SOSEKI proteins might also be involved in apical cell identity specification and division (van Dop et al, 2020).…”