Abstract
Parthenocarpy arises when an ovary develops into fruit without pollination/fertilization. The mechanisms involved in genetic parthenocarpy have attracted attention because of their potential application in plant breeding and also for their elucidation of the mechanisms involved in early fruit development. We have isolated and characterized a novel small parthenocarpic fruit and flower (spff) mutant in the tomato (Solanum lycopersicum) cultivar Micro-Tom. This plant showed both vegetative and reproductive phenotypes including dwarfism of floral organs, male sterility, delayed flowering, altered axillary shoot development, and parthenocarpic production of small fruits. Genome-wide single nucleotide polymorphism array analysis coupled with mapping-by-sequencing using next generation sequencing-based high-throughput approaches resulted in the identification of a candidate locus responsible for the spff mutant phenotype. Subsequent linkage analysis and RNA interference-based silencing indicated that these phenotypes were caused by a loss-of-function mutation of a single gene (Solyc04g077010), which encodes a receptor-like protein kinase that was expressed in vascular bundles in young buds. Cytological and transcriptomic analyses suggested that parthenocarpy in the spff mutant was associated with enlarged ovarian cells and with elevated expression of the gibberellin metabolism gene, GA20ox1. Taken together, our results suggest a role for Solyc04g077010 in male organ development and indicate that loss of this receptor-like protein kinase activity could result in parthenocarpy.
Highlights
The flower-to-fruit transition, known as “fruit set,” corresponds to a major developmental shift that transforms an ovary into a fruit (Gillaspy et al, 1993)
The spff mutant did not produce seeded fruits by practical self-pollination, crossing WT pollen to the spff stigma did result in seeded fruits (Figure 1A); these First filial generation (F1) seeds germinated normally, suggesting that spff is male-sterile, with the ovary retaining substantial fertility
Thirty-three out of 109 Second filial generation (F2) progenies obtained through crossing with the WT cultivar Micro-Tom, and 43 out of 186 F2 progenies obtained through crossing with the WT cultivar Ailsa-Craig, exhibited the spff mutant flower morphology and parthenocarpy phenotypes (Table 1 and Supplementary Figure S2)
Summary
The flower-to-fruit transition, known as “fruit set,” corresponds to a major developmental shift that transforms an ovary into a fruit (Gillaspy et al, 1993). This genetically programmed process is coordinated by a complex network of signaling pathways that are activated by interacting endogenous and exogenous cues, the genetic and molecular factors that control the flower-to-fruit transition remain poorly understood (Ariizumi et al, 2013). The mechanisms underlying the role of the stamen in parthenocarpy have not yet been fully characterized, it has been hypothesized that stamens could counteract fruit set initiation before pollination in tomato plants, and this may be associated in part with elevated levels of GA (Okabe et al, 2019)
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