Occurrence of land‐plant‐specific glycerol‐3‐phosphate acyltransferases is essential for cuticle formation and gametophore development in Physcomitrella patens

Abstract

Summary During the evolution of land plants from aquatic to terrestrial environments, their aerial surfaces were surrounded by cuticle composed of cutin and cuticular waxes to protect them from environmental stresses. Glycerol‐3‐phosphate acyltransferase (GPAT) harboring bifunctional sn‐2 acyltransferase/phosphatase activity produces 2‐monoacylglycerol, a precursor for cutin synthesis. Here, we report that bifunctional sn‐2 GPATs play roles in cuticle biosynthesis and gametophore development of Physcomitrella patens. Land plant‐type cuticle was observed in gametophores but not in protonema. The expression of endoplasmic reticulum‐localized PpGPATs was significantly upregulated in gametophores compared with protonema. Floral organ fusion and permeable cuticle phenotypes of Arabidopsis gpat6‐2 petals were rescued to the wild type (WT) by the expression of PpGPAT2 or PpGPAT4. Disruption of PpGPAT2 and PpGPAT4 caused a significant reduction of total cutin loads, and a prominent decrease in the levels of palmitic and 10,16‐dihydroxydecanoic acids, which are major cutin monomers in gametophores. Δppgpat2 mutants displayed growth retardation, delayed gametophore development, increased cuticular permeability, and reduced tolerance to drought, osmotic and salt stresses compared to the WT. Genome‐wide analysis of genes encoding acyltransferase or phosphatase domains suggested that the occurrence of sn‐2 GPATs with both domains may be a key event in cuticle biogenesis of land plants.

Botrytis cinerea Transcriptome during the Infection Process of the Bryophyte Physcomitrium patens and Angiosperms

“…Penetration pores were detected on the surface of P. patens cell walls and in intercellular spaces that are colonized by infection hyphae that subsequently invaded leaf cells [27]. Cutinases may be involved in gametophore colonization since fungal penetration pegs penetrate the tissues directly through leaf cell walls [53], and protonema cells have no cuticle [76]. In addition, some B. cinerea cutinases show high homology to acetylxylanesterases [77], and could be involved in degradation of xylans in moss tissues.…”

The land plant‐specific MIXTA‐MYB lineage is implicated in the early evolution of the plant cuticle and the colonization of land

“…It was recently reported that K. nitens produces a considerable amount of fatty acids with simple linear carbon chain length from C16 to C18 that attach to cell wall components, when grown on solid medium (Kondo et al ., 2016). Intriguingly, the moss P. patens at the protonema stage produces a smooth hydrophobic layer of only fatty acids, with C16 as a major constituent, that resembles the secretions of K. nitens , while gametophores develop a cutin layer (Lee et al ., 2020). Our observations support the idea that fatty acids were already a well‐established component in the common ancestors of land plants, with the potential to form a more complex polyester matrix by interaction with other well‐known cutin constituents in land plants, including DCAs and HFAs.…”

“…To some extent, this genetic regulatory gene network contains likely orthologues of known genes involved in the cuticle biosynthesis pathway in vascular plants; however, many of the genes and their orthologues have not been functionally analysed in either vascular plants or early‐diverging land plants (Table S7). From this putative MIXTA‐regulated cuticle gene network, so far only GPAT (Lee et al ., 2020) and ABCG (Buda et al ., 2013) have been studied in P. patens , with the function of P. patens CUS only tested in vitro (Yeats et al ., 2014). However, we identified numerous additional putative homologues of cuticle synthesis genes, which lie within the MpSBG9 transcriptional network, but which are functionally uncharacterized.…”

Functional Characterization of Physcomitrella patens Glycerol-3-Phosphate Acyltransferase 9 and an Increase in Seed Oil Content in Arabidopsis by Its Ectopic Expression

“…In this study, we observed the ubiquitous expression of PpGPAT9 during the life cycle of P. patens life (Figure 2). Interestingly, we tried to generate P. patens gpat9 mutants by homologous recombination [35]; however, it was not successful under similar conditions in which knockout mutants of PpGPAT2 and PpGPAT4 involved in cutin synthesis were generated [55]. When PpGPAT9 is overexpressed in Arabidopsis, the total FAME levels increased in PpGPAT9 OX seeds, and alterations in the fatty acid composition of PpGPAT9 OX seeds and leaves were observed when compared with the wild type (Figure 6).…”