Abscisic acid mediated strawberry receptacle ripening involves the interplay of multiple phytohormone signaling networks

Authors: LI, BAI-JUN - Zhejiang University; SHI, YA-NA - Zhejiang University; JAI, HAO-RAN - Zhejiang University; YANG, XIAO-FANG - Zhejiang Academy Of Agricultural Sciences; LU, JIAO - Zhejiang University; Giovannoni, James; JIANG, GUI-HUA - Zhejiang Academy Of Agricultural Sciences; ROSE, JOCELYN - Cornell University; CHEN, KUN-SONG - Zhejiang University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/6/2023
Publication Date: 1/30/2023
Citation: Li, B., Shi, Y., Jai, H., Yang, X., Lu, J., Giovannoni, J.J., Jiang, G., Rose, J., Chen, K. 2023. Abscisic acid mediated strawberry receptacle ripening involves the interplay of multiple phytohormone signaling networks. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2023.1117156.
DOI: https://doi.org/10.3389/fpls.2023.1117156

Interpretive Summary: Fleshy fruits can be classified into those that exhibit either climacteric or non-climacteric ripening: the former type involves a peak of respiration and emission of the gaseous hormone ethylene, which acts as the main regulator of this process, while the latter does not. The phytohormone abscisic acid (ABA) can play either a dominant or supportive role in modulating non-climacteric and climacteric fruit ripening, respectively. Although many studies have reported that the ABA controls non-climacteric fruit ripening and influence fruit quality traits, there is limited understanding of this process compared with that of the much better understood ripening hormone, ethylene, in climacteric fruit. Better elucidation of mechanisms of ABA-mediated fruit ripening has potential for enhancing our understanding of ripening and for developing novel traits and varieties. Here we investigated phytohormone signaling pathways in strawberry ripening mediated by ABA, using gene expression profiling of the fruit at three developmental stages from unripe to ripe and following changes in ABA levels. We identified two key signaling genes (FaSAUR1 and FaSAUR2), shown by genetic manipulation to promote receptacle quality formation.

Technical Abstract: As a canonical non-climacteric fruit, strawberry (Fragaria spp.) ripening is mainly mediated by abscisic acid (ABA), which involves multiple other phytohormone signalings. Many details of these complex associations are not well understood. We present a coexpression network, involving ABA and other phytohormone signalings, based on weighted gene coexpression network analysis of spatiotemporally resolved transcriptome data and phenotypic changes of strawberry receptacles during development and following various treatments. This coexpression network consists of 18,998 transcripts and includes transcripts related to phytohormone signaling pathways, MADS and NAC family transcription factors and biosynthetic pathways associated with fruit quality. Members of eight phytohormone signaling pathways are predicted to participate in ripening and fruit quality attributes mediated by ABA, of which 43 transcripts were screened to consist of the hub phytohormone signalings. In addition to using several genes reported from previous studies to verify the reliability and accuracy of this network, we explored the role of two hub signalings, small auxin up-regulated RNA 1 and 2 in receptacle ripening mediated by ABA, which are also predicted to contribute to fruit quality. These results and publicly accessible datasets provide a valuable resource to elucidate ripening and quality formation mediated by ABA and involves multiple other phytohormone signalings in strawberry receptacle and serve as a model for other non-climacteric fruits.