A genomics approach to understanding the role of auxin in apple (Malus x domestica)fruit size control

Fanny Devoghalaere,Jeannette Keeling,Wendy Payne,Baptiste Guitton,Ga Dayatilake,Kularajathevan Gunaseelan,John James Ross,D Stuart Tustin,Ken C Breen,Toby John Ling,Robert Diak,Evelyne Costes,David Chagné,Ian Charles Hallett,Robert James Schaffer,Karine Myriam David,Thomas Doucen

doi:10.1186/1471-2229-12-7

Abstract

BackgroundAuxin is an important phytohormone for fleshy fruit development, having been shown to be involved in the initial signal for fertilisation, fruit size through the control of cell division and cell expansion, and ripening related events. There is considerable knowledge of auxin-related genes, mostly from work in model species. With the apple genome now available, it is possible to carry out genomics studies on auxin-related genes to identify genes that may play roles in specific stages of apple fruit development.ResultsHigh amounts of auxin in the seed compared with the fruit cortex were observed in 'Royal Gala' apples, with amounts increasing through fruit development. Injection of exogenous auxin into developing apples at the start of cell expansion caused an increase in cell size. An expression analysis screen of auxin-related genes involved in auxin reception, homeostasis, and transcriptional regulation showed complex patterns of expression in each class of gene. Two mapping populations were phenotyped for fruit size over multiple seasons, and multiple quantitative trait loci (QTLs) were observed. One QTL mapped to a region containing an Auxin Response Factor (ARF106). This gene is expressed during cell division and cell expansion stages, consistent with a potential role in the control of fruit size.ConclusionsThe application of exogenous auxin to apples increased cell expansion, suggesting that endogenous auxin concentrations are at least one of the limiting factors controlling fruit size. The expression analysis of ARF106 linked to a strong QTL for fruit weight suggests that the auxin signal regulating fruit size could partially be modulated through the function of this gene. One class of gene (GH3) removes free auxin by conjugation to amino acids. The lower expression of these GH3 genes during rapid fruit expansion is consistent with the apple maximising auxin concentrations at this point.

Highlights

Auxin is an important phytohormone for fleshy fruit development, having been shown to be involved in the initial signal for fertilisation, fruit size through the control of cell division and cell expansion, and ripening related events
To investigate the role of auxin during fruit development, the free IAA amounts were measured at representative times (14, 45, 90 and 132 Days After Full Bloom (DAFB)) during the different fruit development stages in ‘Royal Gala’ fruit cortex and seed
Our work suggests that auxin signals through this cell division/cell expansion phase may be modulated by an ARF gene (ARF106) that is up-regulated during these developmental time points and co-locates with a stable Quantitative Trait Loci (QTL) for fruit weight

Summary

Introduction

Auxin is an important phytohormone for fleshy fruit development, having been shown to be involved in the initial signal for fertilisation, fruit size through the control of cell division and cell expansion, and ripening related events. Work with strawberry and other fruits proposed a mechanism whereby auxin produced by the developing seed regulated fruit growth by controlling firstly cell division and secondly breakdown, conjugation and transport is tightly regulated, leading to auxin homeostasis [6]. Very little is known about the role of GH3 genes during fruit development It has recently been shown in grape that GH3.1 plays a role in the formation of IAA-Asp late during development, coinciding with the onset of ripening [10]. Auxin transport from sites of synthesis to target cells is complex and highly regulated, playing a crucial role in both establishing and changing homeostasis. Auxin is transported both passively through the vasculature and actively through transporters [12]. Mutations in the PIN1 gene lead to pin-like organs with no development of flower parts in Arabidopsis thaliana (Arabidopsis) [13] and members of the PIN family are highly expressed early during tomato fruit development, suggesting a role during fruit set [14]

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