Sterols are required for cell‐fate commitment and maintenance of the stomatal lineage in Arabidopsis

Abstract

SUMMARYAsymmetric cell division is important for regulating cell proliferation and fate determination during stomatal development in plants. Although genes that control asymmetric division and cell differentiation in stomatal development have been reported, regulators controlling the process from asymmetric division to cell differentiation remain poorly understood. Here, we report a weak allele (fk-J3158) of the Arabidopsis sterol C-14 reductase gene FACKEL (FK) that shows clusters of small cells and stomata in leaf epidermis, a common phenomenon that is often seen in mutants defective in stomatal asymmetric division. Interestingly, the physical asymmetry of these divisions appeared to be intact in fk mutants, but the cell-fate asymmetry was greatly disturbed, suggesting that the FK pathway links these two crucial events in the process of asymmetric division. Sterol profile analysis revealed that the fk-J3158 mutation blocked downstream sterol production. Further investigation indicated that cyclopropylsterol isomerase1 (cpi1), sterol 14a-demethylase (cyp51A2) and hydra1 (hyd1) mutants, corresponding to enzymes in the same branch of the sterol biosynthetic pathway, displayed defective stomatal development phenotypes, similar to those observed for fk. Fenpropimorph, an inhibitor of the FK sterol C-14 reductase in Arabidopsis, also caused these abnormal small-cell and stomata phenotypes in wild-type leaves. Genetic experiments demonstrated that sterol biosynthesis is required for correct stomatal patterning, probably through an additional signaling pathway that has yet to be defined. Detailed analyses of time-lapse cell division patterns, stomatal precursor cell division markers and DNA ploidy suggest that sterols are required to properly restrict cell proliferation, asymmetric fate specification, cell-fate commitment and maintenance in the stomatal lineage cells. These events occur after physical asymmetric division of stomatal precursor cells.

Auxin transport and activity regulate stomatal patterning and development

“…The involvement of other auxin transport mechanisms such as ABCBs 16 and PIN-LIKES 34 in stomatal patterning cannot be excluded. Since BFA has also been shown to disrupt sterol trafficking 35 , it can not be ruled out that cell fate abnormalities are solely due to altered auxin transport, especially since the sterol pathway also regulates stomatal patterning 36 . In addition, auxin distribution and signalling restrict the size and promote the dispersion of the stomatal stem cell compartment.…”

Quantitative Genetic Analysis Indicates Natural Selection on Leaf Phenotypes Across Wild Tomato Species (Solanumsect.Lycopersicon; Solanaceae)

“…Stomatal development candidate genes were identified from the well-characterized pathway in Arabidopsis (Pillitteri and Torii 2012) supplemented with additional select candidate genes from sterol and abscisic acid (ABA) biosynthesis pathways. In Arabidopsis, sterol biosynthesis affects stomatal development (Qian et al 2013) through BIN2, which responds to brassinosteroid and phosphorylates multiple stomatal development genes (Gudesblat et al 2012;Kim et al 2012); therefore we included BIN2 orthologs in our analysis. ABA is a stress response hormone that regulates stomatal aperture, but might also regulate stomatal development (Tanaka et al 2013); therefore, we also investigated ABA biosynthetic and catabolic enzymes (Nambara and Marion-Poll 2005).…”

Acyl-CoA-Binding Protein ACBP1 Modulates Sterol Synthesis during Embryogenesis

“…Its catalytic product also is known to regulate polar auxin transport (Mialoundama et al, 2013). Studies on sterol biosynthetic mutants have indicated the existence of other sterol-derived signals that shape plant development, although many remain unknown (Carland et al, 2010;Qian et al, 2013;Zhang et al, 2016).…”