Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis

Abstract

Auxin is an essential hormone, but its biosynthetic routes in plants have not been fully defined. In this paper, we show that the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) family of amino transferases converts tryptophan to indole-3-pyruvate (IPA) and that the YUCCA (YUC) family of flavin monooxygenases participates in converting IPA to indole-3-acetic acid, the main auxin in plants. Both the YUCs and the TAAs have been shown to play essential roles in auxin biosynthesis, but it has been suggested that they participate in two independent pathways. Here, we show that all of the taa mutant phenotypes, including defects in shade avoidance, root resistance to ethylene and N-1-naphthylphthalamic acid (NPA), are phenocopied by inactivating YUC genes. On the other hand, we show that the taa mutants in several known auxin mutant backgrounds, including pid and npy1, mimic all of the well-characterized developmental defects caused by combining yuc mutants with the auxin mutants. Furthermore, we show that overexpression of YUC1 partially suppresses the shade avoidance defects of taa1 and the sterile phenotypes of the weak but not the strong taa mutants. In addition, we discovered that the auxin overproduction phenotypes of YUC overexpression lines are dependent on active TAA genes. Our genetic data show that YUC and TAA work in the same pathway and that YUC is downstream of TAA. The yuc mutants accumulate IPA, and the taa mutants are partially IPA-deficient, indicating that TAAs are responsible for converting tryptophan to IPA, whereas YUCs play an important role in converting IPA to indole-3-acetic acid.

Biosynthesis of the Halogenated Auxin, 4-Chloroindole-3-Acetic Acid

“…The deuterated 4-Cl-IAA was Figure 6. Proposed parallel IAA and 4-Cl-IAA biosynthetic pathways in pea seeds, based on this study and previous evidence (Manabe et al, 1999;Reinecke, 1999;Quittenden et al, 2009;Tivendale et al, 2010;Zhao, 2010;Mashiguchi et al, 2011;Stepanova et al, 2011;Won et al, 2011;Kriechbaumer et al, 2012). IAA does not become chlorinated, and Trp is a point of chlorination.…”

“…There is currently a renewed focus on auxin biosynthesis, due to reports that the YUC proteins do not operate in the tryptamine pathway (Tivendale et al, 2010) but rather the IPyA pathway Stepanova et al, 2011;Won et al, 2011;Kriechbaumer et al, 2012), as suggested previously by Strader and Bartel (2008). However, Mano and Nemoto (2012) recently noted that functional activity for Trp aminotransferases from the IPyA pathway has been demonstrated only for Arabidopsis genes and implied that the IPyA pathway might be restricted to the Brassicaceae.…”

“…In the past, four Trp-dependent IAA biosynthetic pathways have been proposed (Normanly, 2010;Zhao, 2010), but it now appears that one pathway, involving indole-3-pyruvic acid (IPyA), predominates in Arabidopsis Stepanova et al, 2011;Won et al, 2011;Kriechbaumer et al, 2012). Until recently, it was thought that the enzymes involved in converting Trp to IPyA, the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) family (Stepanova et al, 2008;Tao et al, 2008), acted in a separate pathway from the YUCCA (YUC) family (Zhao et al, 2001;Zhao, 2010).…”

“…The YUCs were originally thought to function in the tryptamine pathway, converting tryptamine to N-hydroxytryptamine (Zhao et al, 2001;Expósito-Rodríguez et al, 2007;LeClere et al, 2010). However, the original biochemical function of the YUCs was called into question (Tivendale et al, 2010), and it has now been reported that YUCs act downstream of the TAA family, converting IPyA to IAA Stepanova et al, 2011;Won et al, 2011;Kriechbaumer et al, 2012). Nevertheless, Arabidopsis is known to utilize Brassicaceae-specific biosynthetic pathways (Sugawara et al, 2009), and the IPyA pathway has yet to be demonstrated definitively in species other than Arabidopsis.…”

A Genome-Wide Chronological Study of Gene Expression and Two Histone Modifications, H3K4me3 and H3K9ac, during Developmental Leaf Senescence

“…Of 175 K4-SDRGs that displayed a loss of H3K4me3 marks and decreased gene expression, 13 encoded YUCCA-and SAUR-like genes involved in auxin biosynthesis Stepanova et al, 2011;Won et al, 2011) and response, respectively (Spartz et al, 2012(Spartz et al, , 2014. Auxin synthesis sets in motion major changes in gene expression and physiology (Guilfoyle and Hagen, 2007), and the down-regulation of auxin synthesis and signaling can be considered a primary event in the progression of senescence.…”