ARS | Publication request: Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: March 14, 2010
Publication Date: May 1, 2010
Citation: Leclere, S.L., Schmelz, E.A., Chourey, P.S. 2010. Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiology. 153: 306-318.

Interpretive Summary: In developing seeds, sugars are not only the sole source of carbon but they also modulate many critical processes that are controlled by hormones. Although much is known regarding sugar metabolism very little is known about hormones and, more importantly, the orchestration of sugar and hormone signaling pathways that ultimately determine normal seed development. Using a single gene seed mutation, miniature1 (mn1), which is caused by a major metabolic deficiency in sucrose degradation, we report here changes in the metabolisms of sugar and a major hormone, auxin, in the mutant during seed development. Comparative gene expression analyses to understand the basis of hormone-deficiency in the mutant have led us to show reduced expression levels of a critical auxin biosynthetic gene, Yucca1. Further analyses on the expression of the maize Yucca1 gene in a model plant Arabidopsis confirm our hypothesis that the Yucca1 expression is controlled by sugars. Overall, this study identifies, for the first time, an auxin biosynthetic gene in developing maize seeds, and that its level of expression, and, ultimately, the levels of auxin, is regulated by sugar metabolism. This basic knowledge on sugar-hormone cross-talk is an important factor in seed biology, in particular to engineer sink strength and seed size for increased crop productivity.

Technical Abstract: The Zea mays Mn1 (miniature1) locus encodes the cell wall invertase INCW2, which is localized predominantly in the basal endosperm transfer layer (BETL) of developing kernels and catalyzes conversion of sucrose into glucose and fructose. Mutations in Mn1 result in pleiotropic changes including a reduction in kernel mass and a recently reported decrease in indole-3-acetic acid (IAA) levels throughout kernel development. Here we show mn1-1 basal kernel regions (pedicels and BETL) accumulate higher levels of sucrose and lower levels of glucose and fructose between 8 and 28 days after pollination (DAP) when compared to wild type, whereas upper regions of mn1 accumulate similar or increased concentrations of sugars. To determine the cause of the reduction in IAA accumulation, we investigated transcript levels of several potential IAA biosynthetic enzymes. We demonstrate reduced IAA levels most closely correspond to reduced transcript levels of ZmYUC, a newly identified homolog of the Arabidopsis thaliana gene YUCCA (AtYUC). We further demonstrate that ZmYUC catalyzes the N-hydroxylation of tryptamine, and sugar levels regulate transcript levels of ZmYUC, both in in-vitro cultured kernels and in a promoter-reporter fusion in arabidopsis. These results indicate that developing seed may modulate growth by altering auxin biosynthesis in response to sugar concentrations.