ROP signaling regulates spatial pattern of cell division and specification of meristem notch

Abstract

The formation of cell polarity is essential for many developmental processes such as polar cell growth and spatial patterning of cell division. A plant-specific ROP ( R h o -like GTPases from P lants) subfamily of conserved Rho GTPase plays a crucial role in the regulation of cell polarity. However, the functional study of ROPs in angiosperm is challenging because of their functional redundancy. The Marchantia polymorpha genome encodes a single ROP gene, Mp ROP , providing an excellent genetic system to study ROP-dependent signaling pathways. Mp rop knockout mutants exhibited rhizoid growth defects, and MpROP was localized at the tip of elongating rhizoids, establishing a role for MpROP in the control of polar cell growth and its functional conservation in plants. Furthermore, the Mp rop knockout mutant showed defects in the formation of meristem notches associated with disorganized cell division patterns. These results reveal a critical function of Mp ROP in the regulation of plant development. Interestingly, these phenotypes were complemented not only by Mp ROP but also Arabidopsis At ROP2 , supporting the conservation of ROP’s function among land plants. Our results demonstrate a great potential for M. polymorpha as a powerful genetic system for functional and mechanistic elucidation of ROP signaling pathways during plant development.

Regulation of ROP GTPase cycling between active/inactive states is essential for vegetative organogenesis inMarchantia polymorpha

“…The developmental processes regulated by MpREN and MpROPGAP are diverse, such as tip growth in single cells observed in rhizoid elongation, two-dimensional proliferation of protodermal cells in air-chamber roof expansion, and three-dimensional patterning in gemma development. Considering that the developmental processes regulated by MpREN and MpROPGAP align well with those regulated by MpROP (Rong et al 2022; Mulvey and Dolan 2023), MpROP inactivation by these two RhoGAPs is essential for these processes.…”

“…In M. polymorpha , loss-of-function mutants of Mp ROP failed to form an air chamber containing a roof and air pores (Mulvey and Dolan 2023). This is attributed to the loss of control over the orientation of cell division, especially in the protodermal cell layers near the meristem notch (Rong et al 2022; Mulvey and Dolan 2023). In this study, we demonstrated that the loss of function of Mp REN led to an abnormal orientation of cell division in the protodermal cell layers and the manifestation of an incomplete phenotype in air-chamber roofs equipped with air pores (Figure 4 K, O).…”

“…The genome of M. polymorpha encodes a ROP, a PRONE-type ROPGEF, a DOCK family RhoGEF SPIKE, a ROPGAP, and a REN (PH-GAP). Recently, MpROP 4 was demonstrated to be a key regulator of various developmental processes, including tip growth in rhizoid formation, cell division pattern control in gemma formation, and air chamber development (Rong et al 2022;Mulvey and Dolan 2023). Furthermore, the PRONE-type MpROP activator MpROPGEF (KARAPPO) is essential for the initiation of gemma development (Hiwatashi et al 2019).…”

Rho of plant GTPases with geranylgeranylation motif modulate monoterpene indole alkaloid biosynthesis inCatharanthus roseus

“…Plants contain a varying number of ROPs, ranging from one in Marchantia polymorpha to four in Physcomitrella patens among lower plants, and from four in Pinus taeda (loblolly pine) to eleven in Arabidopsis and thirteen in poplar among higher plants (Rong et al, 2022; Fowler, 2010; Feiguelman et al, 2018). C. roseus has six ROP candidates which are distributed among 4 of the 8 chromosomes in the genome (Figure S1B).…”

“…Moreover, CrROP3 and CrROP5 clearly clustered together with AmRac2 and SdRac2, which positively affect δ-guaiene synthase expression and atropine accumulation, respectively, suggesting that the ROPs from this clade could also be involved in the regulation of specialized metabolic pathways. Notably, clade-1 also includes the sole ROP of M. polymorpha , a bryophyte (Rong et al, 2022), suggesting that the ROP candidates in land plants first originated within this clade.…”