Harbinger transposon insertion in ethylene signaling gene leads to emergence of new sexual forms in cucurbits

Hsin-Ya Huang, Siqi Zhang, Fadi Abou Choucha, Marion Verdenaud, Feng-Quan Tan, Clement Pichot, Hadi Shirazi Parsa, Filip Slavkovic, Qinghe Chen, Christelle Troadec, Fabien Marcel, Catherine Dogimont, Leandro Quadrana, Adnane Boualem and Abdelhafid Bendahmane ()
Additional contact information
Hsin-Ya Huang: Institute of Plant Sciences Paris-Saclay (IPS2)
Siqi Zhang: Institute of Plant Sciences Paris-Saclay (IPS2)
Fadi Abou Choucha: Institute of Plant Sciences Paris-Saclay (IPS2)
Marion Verdenaud: Institute of Plant Sciences Paris-Saclay (IPS2)
Feng-Quan Tan: Institute of Plant Sciences Paris-Saclay (IPS2)
Clement Pichot: Institute of Plant Sciences Paris-Saclay (IPS2)
Hadi Shirazi Parsa: Institute of Plant Sciences Paris-Saclay (IPS2)
Filip Slavkovic: Institute of Plant Sciences Paris-Saclay (IPS2)
Qinghe Chen: Institute of Plant Sciences Paris-Saclay (IPS2)
Christelle Troadec: Institute of Plant Sciences Paris-Saclay (IPS2)
Fabien Marcel: Institute of Plant Sciences Paris-Saclay (IPS2)
Catherine Dogimont: Génétique et Amélioration des Fruits et Légumes (GAFL)
Leandro Quadrana: Institute of Plant Sciences Paris-Saclay (IPS2)
Adnane Boualem: Institute of Plant Sciences Paris-Saclay (IPS2)
Abdelhafid Bendahmane: Institute of Plant Sciences Paris-Saclay (IPS2)

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: Abstract In flowering plants, the predominant sexual morph is hermaphroditism, and the emergence of unisexuality is poorly understood. Using Cucumis melo (melon) as a model system, we explore the mechanisms driving sexual forms. We identify a spontaneous mutant exhibiting a transition from bisexual to unisexual male flower, and identify the causal mutation as a Harbinger transposon impairing the expression of Ethylene Insensitive 2 (CmEIN2) gene. Genetics and transcriptomic analysis reveal a dual role of CmEIN2 in both sex determination and fruit shape formation. Upon expression of CmACS11, EIN2 is recruited to repress the expression of the carpel inhibitor, CmWIP1. Subsequently, EIN2 is recruited to mediate stamina inhibition. Following the sex determination phase, EIN2 promotes fruit shape elongation. Genome-wide analysis reveals that Harbinger transposon mobilization is triggered by environmental cues, and integrates preferentially in active chromatin, particularly within promoter regions. Characterization of a large collection of melon germplasm points to active transpositions in the wild, compared to cultivated accessions. Our study underscores the association between chromatin dynamics and the temporal aspects of mobile genetic element insertions, providing valuable insights into plant adaptation and crop genome evolution.

Date: 2024
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DOI: 10.1038/s41467-024-49250-9

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