Innovation of a Regulatory Mechanism Modulating Semi-determinate Stem Growth through Artificial Selection in Soybean.

Yunfeng Liu,Zhixiang Chen,Jieqing Ping,Dajian Zhang,Shuai Li,Jianxin Ma,Li-Jia Qu

doi:10.1371/journal.pgen.1005818

Yunfeng Liu, Zhixiang Chen + Show 5 more

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https://doi.org/10.1371/journal.pgen.1005818

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Abstract

It has been demonstrated that Terminal Flowering 1 (TFL1) in Arabidopsis and its functional orthologs in other plants specify indeterminate stem growth through their specific expression that represses floral identity genes in shoot apical meristems (SAMs), and that the loss-of-function mutations at these functional counterparts result in the transition of SAMs from the vegetative to reproductive state that is essential for initiation of terminal flowering and thus formation of determinate stems. However, little is known regarding how semi-determinate stems, which produce terminal racemes similar to those observed in determinate plants, are specified in any flowering plants. Here we show that semi-determinacy in soybean is modulated by transcriptional repression of Dt1, the functional ortholog of TFL1, in SAMs. Such repression is fulfilled by recently enabled spatiotemporal expression of Dt2, an ancestral form of the APETALA1/FRUITFULL orthologs, which encodes a MADS-box factor directly binding to the regulatory sequence of Dt1. In addition, Dt2 triggers co-expression of the putative SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (GmSOC1) in SAMs, where GmSOC1 interacts with Dt2, and also directly binds to the Dt1 regulatory sequence. Heterologous expression of Dt2 and Dt1 in determinate (tfl1) Arabidopsis mutants enables creation of semi-determinacy, but the same forms of the two genes in the tfl1 and soc1 background produce indeterminate stems, suggesting that Dt2 and SOC1 both are essential for transcriptional repression of Dt1. Nevertheless, the expression of Dt2 is unable to repress TFL1 in Arabidopsis, further demonstrating the evolutionary novelty of the regulatory mechanism underlying stem growth in soybean.

Highlights

IntroductionStem growth habit is an important morphological and adaptation trait in flowering plants, which is primarily shaped by regulatory processes converting the vegetative shoot apical meristems (SAMs) that form leaves to the inflorescence meristems (IMs) and floral meristems (FMs) that form flowers [1,2,3]
We demonstrate that semideterminacy is originated from an innovation of spatiotemporal expression of an ancient MADS-box gene and consequent changes of spatiotemporal expression of its interacting genes in soybean, which occurred post-domestication of soybean and selected by breeding
The findings from this study provides new insights into the evolutionary novelty of molecular mechanisms regulating stem growth habit reshaped by artificial selection, and exhibited potential application of such an innovative mechanism for molecular design of stem architecture in other crops towards enhanced adaptability and yield potential

Summary

Introduction

Stem growth habit is an important morphological and adaptation trait in flowering plants, which is primarily shaped by regulatory processes converting the vegetative shoot apical meristems (SAMs) that form leaves to the inflorescence meristems (IMs) and floral meristems (FMs) that form flowers [1,2,3]. Such processes have been best studied in Arabidopsis [4, 5]. Both LFY and AP1 are able to bind to the TFL1 locus to suppress its expression in floral meristems [15, 16]

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