Myrosin Idioblast Cell Fate and Development Are Regulated by theArabidopsisTranscription Factor FAMA, the Auxin Pathway, and Vesicular Trafficking

Abstract

Crucifer shoots harbor a glucosinolate-myrosinase system that defends against insect predation. Arabidopsis thaliana myrosinase (thioglucoside glucohydrolase [TGG]) accumulates in stomata and in myrosin idioblasts (MIs). This work reports that the basic helix-loop-helix transcription factor FAMA that is key to stomatal development is also expressed in MIs. The loss of FAMA function abolishes MI fate as well as the expression of the myrosinase genes TGG1 and TGG2. MI cells have previously been reported to be located in the phloem. Instead, we found that MIs arise from the ground meristem rather than provascular tissues and thus are not homologous with phloem. Moreover, MI patterning and morphogenesis are abnormal when the function of the ARF-GEF gene GNOM is lost as well as when auxin efflux and vesicular trafficking are chemically disrupted. Stomata and MI cells constitute part of a wider system that reduces plant predation, the so-called "mustard oil bomb," in which vacuole breakage in cells harboring myrosinase and glucosinolate yields a brew toxic to many animals, especially insects. This identification of the gene that confers the fate of MIs, as well as stomata, might facilitate the development of strategies for engineering crops to mitigate predation.

Myrosin cells are differentiated directly from ground meristem cells and are developmentally independent of the vasculature in Arabidopsis leaves

“…Considering that the master regulator of myrosin cell development, FAMA, is expressed in cells morphologically indistinguishable from neighboring ground meristem cells, 15,16 we conclude that myrosin cells are directly differentiated from ground meristem cells (Fig. 3).…”

“…[26][27][28][29][30] Unlike FAMA, SPCH and MUTE are not required for myrosin cell development. 15,16 However, the entry of ground meristem cells into the myrosin cell lineage may be regulated by yet unknown factor(s) that are expressed prior to FAMA. Consequently, a forward genetic approach would be useful to isolate the unknown factor(s) and may provide insight into the mechanism underlying myrosin cell differentiation.…”

“…15,16 In the inner tissues of leaf primordia, cells that express FAMA are morphologically indistinguishable from neighboring ground meristem cells, 15,16 which are known to be mother cells of all inner leaf cells, including vascular precursor cells. [17][18][19] The expression pattern of FAMA differs from those of vascular precursor genes.…”

“…[17][18][19] The expression pattern of FAMA differs from those of vascular precursor genes. 15,16 To determine whether myrosin cells are differentiated independent of vascular cells, in this study, we simultaneously examined expression patterns of a myrosin cell reporter and vascular precursor reporters. The present results demonstrate that myrosin cells are differentiated directly from ground meristem cells rather than vascular precursor cells.…”

Myrosin Cell Development Is Regulated by Endocytosis Machinery and PIN1 Polarity in Leaf Primordia ofArabidopsis thaliana

“…These results also suggest that auxin accumulation and/or flux levels regulate myrosin cell development. Recently, the activation of an auxin response reporter, ProDR5rev:3XVENUS-N7, was transiently observed in the developing myrosin cells, but not in ground meristem cells (Li and Sack, 2014). This result implies that the polar PIN-dependent transient accumulation of auxin regulates determination of ground meristem cells into myrosin lineage cells through auxin influx from neighboring cells and/or efflux from developing myrosin cells.…”