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Loss-of-Function of a Tomato Receptor-Like Kinase Impairs Male Fertility and Induces Parthenocarpic Fruit Set.

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.

SUBMITTER: Takei H

PROVIDER: S-EPMC6477066 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Parthenocarpic tomato can set fruit and develop without pollination and exogenous hormone treatments under unfavorable environmental conditions, which is beneficial to tomato production from late fall to early spring in greenhouses. In this study, the endogenous hormones in the ovaries of the parthenocarpic tomato line "R35-P" (stigma removed or self-pollination) and the non-parthenocarpic tomato line "R35-N" (self-pollination) at four stages between preanthesis and postanthesis investigated, using high-performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS). A nearly twofold IAA (indoleacetic acid) content was found in "R35-P" rather than in "R35-N" at -2 and 0 days after anthesis (DAA). Except at -2 DAA, a lower ABA (abscisic acid) content was observed in Pe (stigma removed in "R35-P") compared to that in Ps (self-pollination in "R35-P") or CK (self-pollination in "R35-N"). After pollination, although the content of GA1 (gibberellins acid 1) in CK increased, the levels of GAs (gibberellins acids) were notably low. At all four stages, a lower SA (salicylic acid) content was found in Ps and CK than in Pe, while the content and the change trend were similar in Ps and CK. The variation tendencies of JA (jasmonic acid) varied among Pe, Ps, and CK at the studied periods. Furthermore, KEGG (Kyoto Encyclopedia of Genes and Genomes) enrichment analyses of transcriptomic data identified 175 differentially expressed genes (DEGs) related to plant hormone signal transduction, including 63 auxin-related genes, 27 abscisic acid-related genes, 22 ethylene-related genes, 16 cytokinin-related genes, 16 salicylic acid-related genes, 14 brassinosteroid-related genes, 13 jasmonic acid-related genes, and 4 gibberellin-related genes at -2 DAA and 0 DAA. Our results suggest that the fate of a fruit set or degeneration occurred before anthesis in tomato. Auxins, whose levels were independent of pollination and fertilization, play prominent roles in controlling a fruit set in "R35-P," and other hormones are integrated in a synergistic or antagonistic way.

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Loss-of-Function of a Tomato Receptor-Like Kinase Impairs Male Fertility and Induces Parthenocarpic Fruit Set.

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