Arabidopsis thaliana AUCSIA-1 Regulates Auxin Biology and Physically Interacts with a Kinesin-Related Protein

Barbara Molesini,Angelo Spena,Tiziana Pandolfini,Arthur Korte,Youry Pii,Abidur Rahman

doi:10.1371/journal.pone.0041327

Abstract

Aucsia is a green plant gene family encoding 44–54 amino acids long miniproteins. The sequenced genomes of most land plants contain two Aucsia genes. RNA interference of both tomato (Solanum lycopersicum) Aucsia genes (SlAucsia-1 and SlAucsia-2) altered auxin sensitivity, auxin transport and distribution; it caused parthenocarpic development of the fruit and other auxin-related morphological changes. Here we present data showing that the Aucsia-1 gene of Arabidopsis thaliana alters, by itself, root auxin biology and that the AtAUCSIA-1 miniprotein physically interacts with a kinesin-related protein. The AtAucsia-1 gene is ubiquitously expressed, although its expression is higher in roots and inflorescences in comparison to stems and leaves. Two allelic mutants for AtAucsia-1 gene did not display visible root morphological alterations; however both basipetal and acropetal indole-3-acetic acid (IAA) root transport was reduced as compared with wild-type plants. The transcript steady state levels of the auxin efflux transporters ATP BINDING CASSETTE subfamily B (ABCB) ABCB1, ABCB4 and ABCB19 were reduced in ataucsia-1 plants. In ataucsia-1 mutant, lateral root growth showed an altered response to i) exogenous auxin, ii) an inhibitor of polar auxin transport and iii) ethylene. Overexpression of AtAucsia-1 inhibited primary root growth. In vitro and in vivo protein-protein interaction experiments showed that AtAUCSIA-1 interacts with a 185 amino acids long fragment belonging to a 2712 amino acids long protein of unknown function (At4g31570). Bioinformatics analysis indicates that the AtAUCSIA-1 interacting protein (AtAUCSIA-1IP) clusters with a group of CENP-E kinesin-related proteins. Gene ontology predictions for the two proteins are consistent with the hypothesis that the AtAUCSIA-1/AtAUCSIA-1IP complex is involved in the regulation of the cytoskeleton dynamics underlying auxin biology.

Highlights

The Aucsia gene family has been discovered and functionally identified in tomato (Solanum lycopersicum) by showing its role in both vegetative and reproductive development [1]
To identify the biological role of AtAucsia-1, we have searched for null mutants instead of using an approach based on RNA interference (RNAi)
Since ataucsia-1 mutants are impaired in polar auxin transport (PAT) as compared with wild-type, we investigated the effect of ataucsia-1 mutation on primary and lateral root growth in the presence or absence of exogenous auxin

Summary

Introduction

The Aucsia gene family has been discovered and functionally identified in tomato (Solanum lycopersicum) by showing its role in both vegetative and reproductive development [1]. The analysis of Aucsia-silenced tomato plants demonstrated that Aucsia genes have a role in fruit initiation, leaf development, adventitious root formation and root growth [1]. Aucsia-silenced tomato plants showed a reduced polar auxin transport (PAT) in the roots and displayed modifications related to a modified content and/or distribution of auxin, such as an altered sensitivity to the PAT inhibitor N-1-napthylphthalamic acid (1-NPA), reduced rhizogenesis in response to auxin, parthenocarpic development of the fruit and morphological alterations of the leaves [1]. The predominant form of auxin is indole-3acetic acid (IAA), a simple molecule that during green plant evolution became locally synthesized [4] and transported from cell to cell via polar transport [5]. IAA is transported passively with the phloem sap, but it is PAT to be biologically relevant [5,7]

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Conclusion