Antagonistic Gene Activities Determine the Formation of Pattern Elements along the Mediolateral Axis of the Arabidopsis Fruit

Santiago González-Reig,Antonio Martínez-Laborda,Martin F Yanofsky,Antonio Vera,Juan José Ripoll,Li-Jia Qu

doi:10.1371/journal.pgen.1003020

Santiago González-Reig, Antonio Martínez-Laborda + Show 4 more

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https://doi.org/10.1371/journal.pgen.1003020

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Abstract

The Arabidopsis fruit mainly consists of a mature ovary that shows three well defined territories that are pattern elements along the mediolateral axis: the replum, located at the medial plane of the flower, and the valve and the valve margin, both of lateral nature. JAG/FIL activity, which includes the combined functions of JAGGED (JAG), FILAMENTOUS FLOWER (FIL), and YABBY3 (YAB3), contributes to the formation of the two lateral pattern elements, whereas the cooperating genes BREVIPEDICELLUS (BP) and REPLUMLESS (RPL) promote replum development. A recent model to explain pattern formation along the mediolateral axis hypothesizes that JAG/FIL activity and BP/RPL function as antagonistic lateral and medial factors, respectively, which tend to repress each other. In this work, we demonstrate the existence of mutual exclusion mechanisms between both kinds of factors, and how this determines the formation and size of the three territories. Medial factors autonomously constrain lateral factors so that they only express outside the replum, and lateral factors negatively regulate the medially expressed BP gene in a non-autonomous fashion to ensure correct replum development. We also have found that ASYMMETRIC LEAVES1 (AS1), previously shown to repress BP both in leaves and ovaries, collaborates with JAG/FIL activity, preventing its repression by BP and showing synergistic interactions with JAG/FIL activity genes. Therefore AS gene function (the function of the interacting genes AS1 and AS2) has been incorporated in the model as a new lateral factor. Our model of antagonistic factors provides explanation for mutant fruit phenotypes in Arabidopsis and also may help to understand natural variation of fruit shape in Brassicaceae and other species, since subtle changes in gene expression may cause conspicuous changes in the size of the different tissue types.

Highlights

The fruit, a pivotal structure in angiosperms, is the specialized plant organ that develops from the gynoecium after fertilization of the ovules
We have previously demonstrated that the MYB transcription factor ASYMMETRIC LEAVES1 (AS1) regulates patterning along the mediolateral axis of the Arabidopsis fruit
We previously found that the as1 fruit phenotype was largely associated with the misregulation of BP, because: 1) 35S::BP had the same fruit alterations as seen in as1 plants, 2) BP was ectopically expressed in lateral regions of as1 pistils and 3) in as1 bp fruits, replum and valves almost completely recovered the wildtype size [19]

Summary

Introduction

The fruit, a pivotal structure in angiosperms, is the specialized plant organ that develops from the gynoecium after fertilization of the ovules. The very term angiosperm comes from the Greek and means ‘‘seeds enclosed in a vessel’’ (angion, vessel, and sperma, seed), describing the main functions of this organ: seed protection and dispersal. Our present knowledge on fruit development principally derives from research in the crucifer Arabidopsis thaliana, Arabidopsis hereafter [1,2,3,4,5,6,7]. All the tissues of the Arabidopsis fruit are already present in the bicarpelate pistil, whose development is initiated as a group of cells that form a dome-shaped primordium. For instance, along the apical-basal axis both pistils and fruits show, from bottom to top, the basal gynophore, the ovary, the style and the apical stigma (Figure 1A)

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