A common genetic mechanism underlies morphological diversity in fruits and other plant organs

Shan Wu,Aurora Díaz,Yiqun Weng,Neda Keyhaninejad,Biyao Zhang,Dennis Halterman,Eudald Illa-Berenguer,Tea Meulia,Yupeng Pan,Herman J Van Eck ,Hyun Jung Kim,C Robin Buell,Nathan K Taitano ,Shelley Jansky ,Johan H Willemsen ,Antonio J Monforte,Manohar Chakrabarti,Gustavo Rodríguez ,María José Gonzalo ,Courtney P Leisner,Esther Van Der Knaap

doi:10.1038/s41467-018-07216-8

Abstract

Shapes of edible plant organs vary dramatically among and within crop plants. To explain and ultimately employ this variation towards crop improvement, we determined the genetic, molecular and cellular bases of fruit shape diversity in tomato. Through positional cloning, protein interaction studies, and genome editing, we report that OVATE Family Proteins and TONNEAU1 Recruiting Motif proteins regulate cell division patterns in ovary development to alter final fruit shape. The physical interactions between the members of these two families are necessary for dynamic relocalization of the protein complexes to different cellular compartments when expressed in tobacco leaf cells. Together with data from other domesticated crops and model plant species, the protein interaction studies provide possible mechanistic insights into the regulation of morphological variation in plants and a framework that may apply to organ growth in all plant species.

Highlights

Shapes of edible plant organs vary dramatically among and within crop plants
Consistent with the co-localization experiments, the Bifluorescence Complementation (BiFC) signal in the tobacco leaf cells was substantially reduced when coexpressing mutant versions of the proteins. These results demonstrate that both SlOFPs and SlTRMs physically interact in plant cells and that this contact leads to relocalization of one or the other protein
In addition to providing evidence that OVATE Family Protein (OFP) and TONNEAU1 Recruiting Motif (TRM) control fruit, tuber, vegetable, and grain shapes in domesticated plants and were the targets of selection, our findings uncovered a link between these two families which are common in genomes of multicellular plants[11,24]

Summary

Introduction

Shapes of edible plant organs vary dramatically among and within crop plants. To explain and employ this variation towards crop improvement, we determined the genetic, molecular and cellular bases of fruit shape diversity in tomato. Protein interaction studies, and genome editing, we report that OVATE Family Proteins and TONNEAU1 Recruiting Motif proteins regulate cell division patterns in ovary development to alter final fruit shape. Gaining insights into the function of these proteins in developmental processes related to shape determination will be key to understanding the remarkable morphological diversity observed in plant organs within and among species. We demonstrate that members of the same OFP and TRM subclades are associated with natural variation of melon and cucumber fruit as well as potato tuber shape These results integrate the previous knowledge on OFPs and TRMs, and provide possible mechanistic insights into organ shape regulation in higher plants

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Results

Conclusion