Modulation of Asymmetric Division Diversity through Cytokinin and SPEECHLESS Regulatory Interactions in the Arabidopsis Stomatal Lineage

Abstract

Coordinated growth of organs requires communication among cells within and between tissues. In plants, leaf growth is largely dictated by the epidermis; here, asymmetric and self-renewing divisions of the stomatal lineage create two essential cell types-pavement cells and guard cells-in proportions reflecting inputs from local, systemic, and environmental cues. The transcription factor SPEECHLESS (SPCH) is the prime regulator of divisions, but whether and how it is influenced by external cues to provide flexible development is enigmatic. Here, we show that the phytohormone cytokinin (CK) can act as an endogenous signal to affect the extent and types of stomatal lineage divisions and forms a regulatory circuit with SPCH. Local domains of low CK signaling are created by SPCH-dependent cell-type-specific activity of two repressive type-A ARABIDOPSIS RESPONSE REGULATORs (ARRs), ARR16 and ARR17, and two secreted peptides, CLE9 and CLE10, which, together with SPCH, can customize epidermal cell-type composition.

A Plant-Specific Polarity Module Establishes Cell Fate Asymmetry in the Arabidopsis Stomatal Lineage

“…POLAR, through its binding of BIN2, changes the nuclear/cytoplasmic balance of the latter, with consequences to MAPK signaling and ultimately to the stability of SPCH in meristemoids post-division (Houbaert et al, 2018). Both MAPK and BIN2-related signaling cascades are used in a large number of developmental and physiological events, and other scaffolds have been identified, perhaps most interesting among them is OCTOPUS (OPS) that, similar to POLAR, sequesters BIN2 away from the nucleus from its a polarized plasma-membrane location in protophloem cells (Vatén et al, 2018). A question that remains, however, is whether polar cortical localization is only a means to ensuring segregation during division (BASL/MAPK) or sequestration from the nucleus (POLAR or OPS/BIN2), or whether polarization there are activities that must take place in a restricted region of the cortex of developing cells.…”

SPEECHLESS Speaks Loudly in Stomatal Development

“…Unlike the negative regulation of SPCH by MAPK-and BIN2-mediated phosphorylation, CDKA;1 mediated phosphorylation of SPCH at Serine 186 promotes stomatal initiation, revealing that SPCH activity and stability are fine-tuned via phosphorylation by multiple kinases in response to various signals (Yang et al, 2015) (Figure 2). Increased cytokinin (CK) levels or signaling promotes SPCH expression, and SPCH directly induces the expression of the type-A ARABIDOPSIS RESPONSE REGULATOR16 (ARR16) and CLAVATA3/ EMBRYO SURROUNDING REGION RELATED 9/10 (CLE9/ 10) (Lau et al, 2014;Vaten et al, 2018). ARR16 negatively regulates CK response and CLE9/10 represses type-A ARRs.…”

“…ARR16 negatively regulates CK response and CLE9/10 represses type-A ARRs. The SPCH-dependent activities of the repressive type-A ARR16/17 and the secreted peptides CLE9/10 are essential for establishing local domains of low CK signaling, which inhibits both SLGC division and stomatal formation (Vaten et al, 2018). ARR16/17 and CLE9/ 10 counteract the proliferative effect of SPCH to customize the epidermal cell-type composition (Vaten et al, 2018).…”

“…The SPCH-dependent activities of the repressive type-A ARR16/17 and the secreted peptides CLE9/10 are essential for establishing local domains of low CK signaling, which inhibits both SLGC division and stomatal formation (Vaten et al, 2018). ARR16/17 and CLE9/ 10 counteract the proliferative effect of SPCH to customize the epidermal cell-type composition (Vaten et al, 2018). CLE9/10 peptides are also recognized by the receptor kinase HAESA-LIKE 1 (HSL1) to regulate the stomatal lineage cell division; however, the underlying mechanism is unknown (Qian et al, 2018).…”

Form, development and function of grass stomata

“…Also Arabidopsis meristemoids exhibit strong asymmetry and polarity, which seems to be important for stomatal spacing and patterning (Lau and Bergmann, 2012;Pillitteri and Torii, 2012), and creates flexibility regarding the relative numbers of stomata and pavement cells, a process modulated by cytokinin (Vat en et al, 2018). Meristemoid polarity in Arabidopsis involves BREAKING OF ASYMME-TRY IN THE STOMATAL LINEAGE (AtBASL; Dong et al, 2009), BREVIS RADIX (AtBRX)-like family genes (Rowe et al, 2019) and AtPOLAR family genes (Houbaert et al, 2018).…”