Regulatory Features Underlying Pollination-Dependent and -Independent Tomato Fruit Set Revealed by Transcript and Primary Metabolite Profiling

Abstract

Indole Acetic Acid 9 (IAA9) is a negative auxin response regulator belonging to the Aux/IAA transcription factor gene family whose downregulation triggers fruit set before pollination, thus giving rise to parthenocarpy. In situ hybridization experiments revealed that a tissue-specific gradient of IAA9 expression is established during flower development, the release of which upon pollination triggers the initiation of fruit development. Comparative transcriptome and targeted metabolome analysis uncovered important features of the molecular events underlying pollination-induced and pollination-independent fruit set. Comprehensive transcriptomic profiling identified a high number of genes common to both types of fruit set, among which only a small subset are dependent on IAA9 regulation. The fine-tuning of Aux/IAA and ARF genes and the downregulation of TAG1 and TAGL6 MADS box genes are instrumental in triggering the fruit set program. Auxin and ethylene emerged as the most active signaling hormones involved in the flower-to-fruit transition. However, while these hormones affected only a small number of transcriptional events, dramatic shifts were observed at the metabolic and developmental levels. The activation of photosynthesis and sucrose metabolism-related genes is an integral regulatory component of fruit set process. The combined results allow a far greater comprehension of the regulatory and metabolic events controlling early fruit development both in the presence and absence of pollination/fertilization.

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

“…Moreover, the link between auxin biosynthesis or signaling and sugar accumulation in the fruit tissues has been highlighted by a number of studies (Pandolfini et al, 2002;Wang et al, 2009), though the mechanisms by which this hormone impacts sugar metabolism and therefore fruit quality remain poorly understood. Previous work demonstrated that DR12/ARF4, a member of the tomato ARF gene family of transcription factors, is involved in the regulation of fruit development; that is, transgenic tomato plants with decreased SlARF4 mRNA levels produced dark-green fruit at immature stages, with increased chlorophyll content, a larger number of chloroplasts, and unusual cell division at late stages of fruit development, as well as blotchy ripening and enhanced fruit firmness (Jones et al, 2002;Guillon et al, 2008).…”

Comprehensive Tissue-Specific Transcriptome Analysis Reveals Distinct Regulatory Programs during Early Tomato Fruit Development

“…Previous studies have revealed complex patterns of gene expression during tomato fruit set and early growth, with prominent modulation of gene expression related to cell division, photosynthesis, sugar metabolism, and hormone biology, and hinted at the existence of distinct regulatory programs associated with specialized tissue development (Lemaire-Chamley et al, 2005;Vriezen et al, 2008;Mounet et al, 2009;Wang et al, 2009).…”

“…While previous transcriptomic studies have suggested distinct expression profiles in different parts of the fruit, they have typically lacked tissue specificity, being performed on whole ovaries and fruit (Wang et al, 2009) or using relatively coarse manual dissection (Lemaire-Chamley et al, 2005;Vriezen et al, 2008).…”

Role of cis-12-Oxo-Phytodienoic Acid in Tomato Embryo Development

“…This repeatedly described communication is necessary for proper seed development and involves auxin and ethylene as preferential signals (Balbi and Lomax, 2003;Wang et al, 2009). It might be, however, negatively affected by insufficient levels of OPDA.…”