The TomatoAux/IAATranscription FactorIAA9Is Involved in Fruit Development and Leaf Morphogenesis

Abstract

Auxin/indole-3-acetic acid (Aux/IAA) proteins are transcriptional regulators that mediate many aspects of plant responses to auxin. While functions of most Aux/IAAs have been defined mainly by gain-of-function mutant alleles in Arabidopsis thaliana, phenotypes associated with loss-of-function mutations have been scarce and subtle. We report here that the downregulation of IAA9, a tomato (Solanum lycopersicum) gene from a distinct subfamily of Aux/IAA genes, results in a pleiotropic phenotype, consistent with its ubiquitous expression pattern. IAA9-inhibited lines have simple leaves instead of wild-type compound leaves, and fruit development is triggered before fertilization, giving rise to parthenocarpy. This indicates that IAA9 is a key mediator of leaf morphogenesis and fruit set. In addition, antisense plants displayed auxin-related growth alterations, including enhanced hypocotyl/stem elongation, increased leaf vascularization, and reduced apical dominance. Auxin dose-response assays revealed that IAA9 downregulated lines were hypersensitive to auxin, although the only early auxin-responsive gene that was found to be upregulated in the antisense lines was IAA3. The activity of the IAA3 promoter was stimulated in the IAA9 antisense genetic background, indicating that IAA9 acts in planta as a transcriptional repressor of auxin signaling. While no mutation in any member of subfamily IV has been reported to date, the phenotypes associated with the downregulation of IAA9 reveal distinct and novel roles for members of the Aux/IAA gene family. INTRODUCTIONThe phytohormone auxin is central to a myriad of aspects of plant growth and developmental processes. At the cellular level, auxin controls cell division, extension, and differentiation. On a wholeplant level, auxin plays an essential role in processes such as apical dominance, lateral/adventitious root formation, tropisms, fruit set and development, vascular differentiation, and embryogenesis (Friml, 2003). While it is clear that auxin plays a pivotal role in plant growth and development, the molecular effectors by which this hormone exerts its effect are still relatively unknown. For example, in the process of fruit set, the onset of ovary development into fruit and its subsequent development are naturally triggered by signals from successful fertilization. These processes can be initiated in the absence of pollination and fertilization by exogenous auxin or auxin transport inhibitors (Gustafson, 1937;Beyer and Quebedeaux, 1974) or by the ovaryspecific expression of Agrobacterium tumefaciens indoleacetamide monoxygenase (iaaM) or root loci B (rolB) genes, which confer higher auxin production or increased auxin sensitivity, respectively (Ficcadenti et al., 1999;Carmi et al., 2003). The molecular mediators by which auxin impacts this process are still unknown.The recent discovery that the F-box protein Transport Inhibitor Response1 functions as an auxin receptor represents a major breakthrough (Dharmasiri et al., 2005;Kepinski and Leyser, 2005) in understanding ho...

SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development

“…Yet, the prevailing idea is that fruit growth and metabolism are predominantly supported by photoassimilate supply from the source (Ruan et al, 2012), and in this regard, our data cannot rule out that the higher sugar content observed in the transgenic lines could also arise from a more efficient import of photoassimilate into fruit. Indeed, altering auxin sensitivity via down-regulation of tomato IAA9 has been reported to promote the development of vascular bundles (Wang et al, 2005), which may enhance sink strength and sugar supply to the fruit.…”

“…These two fragments were then cloned into the pGA643 binary vector in the antisense orientation under the transcriptional control of the Cauliflower mosaic virus 35S (35SCaMV) promoter and the nopaline synthase terminator. All transgenic plants were generated by Agrobacterium tumefaciens-mediated transformation according to Wang et al (2005). All experiments were carried out using homozygous lines from F3 or later generations.…”

“…Taken together, these findings suggest the ability of auxin to regulate sugar accumulation during fruit development via SlARF4. A number of studies have demonstrated the role of specific ARFs in early stages of fruit development such as fruit set (Wang et al, 2005;Goetz et al, 2006;de Jong et al, 2009b), but the putative role of these transcriptional regulators in controlling some ripening-related events and the overall quality of the fruit remains largely unknown.…”

“…However, with the exception of ethylene, which has been shown to control many ripening-associated metabolic pathways such as those leading to pigment and aroma volatile production, the impact of other hormones on fruit quality traits remains poorly known (Pech et al, 2012). Auxin is, however, an important phytohormone for initiation of fleshy fruit development, since it was shown to play a key role in triggering fruit set upon flower fertilization (Pandolfini et al, 2002;Wang et al, 2005;de Jong et al, 2009ade Jong et al, , 2009b. Auxin is also essential in determining final fruit size through the control of cell division and cell expansion (Devoghalaere et al, 2012).…”

Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1

“…For instance, it was shown that expression of a GA 20-oxidase gene was induced by pollination in tomato (Rebers et al 1999;Serrani et al 2007), and the importance of SlDELLA, which represses GA signaling and tomato fruit set, has also been demonstrated (Marti et al 2007). In additional, IAA9 and ARF8, both transcriptional regulators of the auxin response, were shown to be part of an important signal for fruit set (Wang et al 2005;Goetz et al 2007). However, many other genes remain to be discovered and investigated.…”