Proteomic insight into fruit set of cucumber (Cucumis sativus L.) suggests the cues of hormone-independent parthenocarpy

Abstract

BackgroundParthenocarpy is an excellent agronomic trait that enables crops to set fruit in the absence of pollination and fertilization, and therefore to produce seedless fruit. Although parthenocarpy is widely recognized as a hormone-dependent process, hormone-insensitive parthenocarpy can also be observed in cucumber; however, its mechanism is poorly understood. To improve the global understanding of parthenocarpy and address the hormone-insensitive parthenocarpy shown in cucumber, we conducted a physiological and proteomic analysis of differently developed fruits.ResultsPhysiological analysis indicated that the natural hormone-insensitive parthenocarpy of ‘EC1’ has broad hormone-inhibitor resistance, and the endogenous hormones in the natural parthenocarpy (NP) fruits were stable and relatively lower than those of the non-parthenocarpic cultivar ‘8419 s-1.’ Based on the iTRAQ technique, 683 fruit developmental proteins were identified from NP, cytokinin-induced parthenocarpic (CP), pollinated and unpollinated fruits. Gene Ontology (GO) analysis showed that proteins detected from both set and aborted fruits were involved in similar biological processes, such as cell growth, the cell cycle, cell death and communication. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that ‘protein synthesis’ was the major biological process that differed between fruit set and fruit abortion. Clustering analysis revealed that different protein expression patterns were involved in CP and NP fruits. Forty-one parthenocarpy-specialized DEPs (differentially expressed proteins) were screened and divided into two distinctive groups: NP-specialized proteins and CP-specialized proteins. Furthermore, qRT-PCR and western blot analysis indicated that NP-specialized proteins showed hormone- or hormone-inhibitor insensitive expression patterns in both ovaries and seedlings.ConclusionsIn this study, the global molecular regulation of fruit development in cucumber was revealed at the protein level. Physiological and proteomic comparisons indicated the presence of hormone-independent parthenocarpy and suppression of fruit abortion in cucumber. The proteomic analysis suggested that hormone-independent parthenocarpy is regulated by hormone-insensitive proteins such as the NP-specialized proteins. Moreover, the regulation of fruit abortion suppression may be closely related to protein synthesis pathways.Electronic supplementary materialThe online version of this article (10.1186/s12864-017-4290-5) contains supplementary material, which is available to authorized users.

Auxin Metabolism Is Involved in Fruit Set and Early Fruit Development in the Parthenocarpic Tomato “R35-P”

“…Parthenocarpy can overcome these problems by converting the ovary into a developing fruit without pollination and exogenous hormone application, thereby producing seedless fruit. Currently, for highly desired agronomic traits, many vegetable crops, such as tomato ( Gorguet et al, 2005 , 2008 ; Takisawa et al, 2017 , 2020 ), cucumber ( Wu et al, 2016 ; Li et al, 2017 ), and eggplant ( Du et al, 2016 ; Chen et al, 2017 ) can naturally produce parthenocarpic fruit. The use of parthenocarpic cultivars is considered to be the most cost-effective solution for a stable fruit set under suboptimal environmental conditions.…”

Serial-Omics and Molecular Function Study Provide Novel Insight into Cucumber Variety Improvement

“…A proteomic study of scion-rootstock graft revealed 50 proteins that were differentially expressed and that those proteins were involved in a wide range of functions, including photosynthesis, carbohydrate metabolism, energy metabolism, and protein metabolism [39]. Cluster analysis showed that 41 parthenocarpy-related, differentially expressed proteins were screened in cytokinin-induced and naturally occurring parthenocarpic fruits, which confirmed that hormone-insensitive proteins can manipulate the mechanism of hormone-independent parthenocarpy [40]. The application of a plant growth-promoting Trichoderma strain (T. longibrachiatum "H9") to cucumber roots resulted in the upregulation of genes and proteins that were mainly involved in defense/stress processes, secondary metabolism, phytohormone synthesis, and signal transduction [41].…”

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

“…Consistent with early observations showing that inhibitors of auxin transport that block movement of auxin out of the ovary can promote parthenocarpy [ 41 ], parthenocarpic cucumbers exhibited decreased transcription of the auxin receptor and signal transport genes CsTIR1 and CsAFB2 [ 42 ]. Interestingly, hormone-insensitive parthenocarpy also has been observed in certain lines of cucumber, possibly resulting from expression of proteins that showed hormone-insensitive patterns in both ovaries and seedlings [ 43 ].…”

“…As is the case for fruit set following pollination, import of sugars is critical for parthenocarpic fruit growth. Increased sugar transport was associated with increased expression of auxin and cytokinin signaling genes suggesting interplay among sugars and plant hormones [ 44 ], and a higher rate of cell division in parthenocarpic fruit was associated with higher carbohydrate metabolism [ 43 ]. In some genetically parthenocarpic lines, especially European greenhouse types, parthenocarpy has been associated with weaker first fruit inhibition (e.g., [ 45 ]), potentially providing a yield advantage.…”