Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis

Abstract

Auxin biosynthesis in plants has remained obscure although auxin has been known for decades as a key regulator for plant growth and development. Here we define the YUC gene family and show unequivocally that four of the 11 predicted YUC flavin monooxygenases (YUC1, YUC2, YUC4, and YUC6) play essential roles in auxin biosynthesis and plant development. The YUC genes are mainly expressed in meristems, young primordia, vascular tissues, and reproductive organs. Overexpression of each YUC gene leads to auxin overproduction, whereas disruption of a single YUC gene causes no obvious developmental defects. However, yuc1yuc4, yuc2yuc6, all of the triple and quadruple mutants of the four YUC genes, display severe defects in floral patterning, vascular formation, and other developmental processes. Furthermore, inactivation of the YUC genes leads to dramatically reduced expression of the auxin reporter DR5-GUS in tissues where the YUC genes are expressed. Moreover, the developmental defects of yuc1yuc4 and yuc1yuc2yuc6 are rescued by tissue-specific expression of the bacterial auxin biosynthesis gene iaaM, but not by exogenous auxin, demonstrating that spatially and temporally regulated auxin biosynthesis by the YUC genes is essential for the formation of floral organs and vascular tissues.[Keywords: Auxin; auxin biosynthesis; flavin monooxygenase; flower development; vascular development] Supplemental material is available at http://www.genesdev.org.

TheTRANSPORT INHIBITOR RESPONSE2Gene Is Required for Auxin Synthesis and Diverse Aspects of Plant Development

“…Localized changes in auxin level are known to play a key role in embryogenesis, meristem establishment and maintenance, organogenesis, and tropic growth. The role of auxin transport during these processes is well established, but information on the role of auxin synthesis in the regulation of auxin flux is just beginning to emerge (Cheng et al, 2006;Stepanova et al, 2008;Tao et al, 2008). Expression of the TIR2/TAA1 gene is spatially restricted during embryo development, and seedling development is consistent with existing models (this study; Stepanova et al, 2008;Tao et al, 2008).…”

“…the TAM pathway and the IPA pathway (Cheng et al, 2006;Stepanova et al, 2008;Tao et al, 2008). Although the pathways may be partially redundant, their precise role in various aspects of plant development remains to be fully explored.…”

A transcriptional view on somatic embryogenesis

“…The importance of endogenous auxin production for 2,4‐D‐induced SE was demonstrated using yuc knockout mutants, which show a reduced response in 2,4‐D‐treated secondary somatic embryo cultures (Bai, Su, Yuan, & Zhang, 2013; Wojcikowska et al., 2013), but its significance for LEC‐induced SE is not known. YUC overexpression in seedlings is not sufficient to trigger spontaneous SE in seedlings, but rather induces epinastic cotyledon growth (Cheng, Dai, & Zhao, 2006; Kim et al., 2007; Woodward et al., 2005), a typical auxin overproduction phenotype. This suggests that the competence of the underlying tissue is an important determinant for SE induction.…”

Hormonal Regulation of Branching in Grasses

“…PINFORMED1 (PIN1) encodes one of the auxin efflux carriers (Galweiler et al, 1998), while PINOID (PID) encodes a Ser/Thr protein kinase that phosphorylates and regulates the localization of PIN1 (Christensen et al, 2000;Benjamins et al, 2001;Friml et al, 2004;Michniewicz et al, 2007). Knockout of multiple genes in the YUCCA (YUC) family of flavin monooxygenases also causes a pin phenotype (Cheng et al, 2006). YUC genes are involved in localized auxin biosynthesis, indicating that auxin biosynthesis is also required for floral meristem initiation (Zhao, 2008).…”