Cucumber ovaries inhibited by dominant fruit express a dynamic developmental program, distinct from either senescence‐determined or fruit‐setting ovaries

Abstract

Cucurbits represent an attractive model to explore the dynamics of fruit set, whose regulation is not fully understood, despite its importance for yield determination. A fertilized ovary must integrate signals from distant plant parts and 'decide' whether to set fruit, or remain inhibited and later senesce. Here, we set out to characterize first-fruit inhibition (FFI), that is, the inhibitory effect of the first fruit on subsequent development of younger ovaries during pollination-induced and parthenocarpic fruit set. After the first fertilized ovaries set fruit, younger fertilized ovaries remained in a temporary state of inhibition. Such ovaries preserved their size and green color, and if the older fruit were removed within a 1-week reversibility window, they set fruit. The FFI effect was documented in both fertilized and parthenocarpic ovaries. We compared the gene expression profiles of pollinated ovaries (committed to set fruit) with respect to those affected by FFI, and to non-pollinated ovaries (undergoing senescence). The three fates of the ovaries were characterized by wide changes in gene expression, with several specific transcripts being up- or down-regulated in response to pollination, and to the presence of inhibitory fruit. Metabolic profiling was undertaken and integrated with the transcriptomic data in order to characterize early physiological changes that occur in post-anthesis ovaries in parthenocarpic and non-parthenocarpic genotypes. The combined results are discussed with respect to current models of fruit set and specifically with regard to FFI. Moreover, these metabolome and transcriptome data provide a valuable resource for studying ovary development and fruit set.

Evaluation and Genetic Analysis of Parthenocarpic Germplasms in Cucumber

“…Interestingly, the “tolerance” of first-fruit inhibition was only observed in EG- and UP-type cucumbers ( Figure 3 A), while regarding PFE rates, 46% of NC-type and 66% SC-type cucumbers were below 25% ( Figure 2 D; Table S1 ). Many studies suggested that the inhibition of parthenocarpy fruit expansion caused by the first-fruit inhibition, which should not be ignored during the evaluation of parthenocarpy germplasms [ 23 , 54 , 55 , 56 ]. In recent decades, a series of EG and UP type parthenocarpic germplasms without FFI effects have been identified [ 57 , 58 ], and the parthenocarpy ability of major varieties in American and European countries have been improved using these resources.…”

The ethylene receptors CpETR1A and CpETR2B cooperate in the control of sex determination in Cucurbita pepo

“…In the absence of pollination and fertilization, growth of the ovary is aborted. Fruit set is known to be regulated positively by hormones such as auxins and gibberellins, and negatively by ethylene (Martínez et al , 2013; Shinozaki et al , 2018; Shnaider et al , 2018). Therefore, the reduction of ethylene sensitivity in the etr1a and etr2b mutants could trigger parthenocarpy by delaying flower anthesis and consequently the checking point for fruit set.…”

Morphological and Genetic Diversity of Cucumber (Cucumis sativus L.) Fruit Development

“…Competition for photosynthetic resources also influences fruit growth. First fruit inhibition is a long-recognized phenomenon in cucumber, wherein initial fruit set, either pollinated or parthenocarpic, can inhibit subsequent fruit set or cause a significantly reduced growth rate [ 20 , 21 , 22 ]. Sink activity, including activity of AGA2, accumulation of sucrose, and accumulation of the source–sink signal molecule, trehalose-6-phosphate (T6P), was found to be greater in first fruit than second fruit [ 20 ].…”

“…Extensive metabolic and transcriptional changes were observed within 24 h post-pollination but differed markedly between the first and second fruit. Removal of the first fruit released inhibition of the second fruit, resulting in increased growth rate, sink activity, and a reprogramming of the metabolome to resemble early post-pollination in a non-inhibited fruit [ 20 , 21 ].…”