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The miR156x + p/SPL13-6 module responds to ABA, IAA, and ethylene, and SPL13-6 participates in the juvenile–adult phase transition in Pyrus

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Abstract

Perennial woody fruit trees usually have a long juvenile period, which greatly restricts the breeding process. The miR156/squamosa promoter binding protein-like (SPL) module and hormones participate in phase transition. To determine which miR156s and SPLs play roles in the juvenile–adult phase transition in pear (Pyrus) trees, and whether hormones affect the expressions of miR156 and target SPLs, we constructed and sequenced juvenile and adult sRNA libraries and then analyzed the expression patterns of differentially expressed miRNAs/targets pairs in the process of ontogenic development as well as under abscisic acid (ABA), indole-3-acetic acid (IAA) and ethylene precursor 1-aminocylopropane-1-carboxylic acid (ACC) treatments. SPL13-6 was identified as a candidate gene, and the function of its product was verified in transgenic Arabidopsis. Compared with in the juvenile phase, 65/62 miRNAs were up-/down-regulated in the adult phase, including two miR156 members, miR156x and miR156p. According to the mRNA database for the juvenile–adult phase transition, 11 pairs of miRNAs/targets participate in the juvenile–adult phase transition, including four pairs of miR156/SPLs. With ontogenic development, the expression level of miR156x + p decreased and those of four SPLs increased. ABA and IAA inhibited the expression of miR156, while low and high concentrations of ACC increased and decreased miR156 expression, respectively, compared with control levels. Among the four SPLs, SPL13-6 displayed an opposite expression patterns compared with that of miR156 under hormone treatments. Overexpression of SPL13-6 in Arabidopsis resulted in earlier abaxial trichome production and flowering phenotypes compared with the wild-type phenotype. These results suggest that the miR156x + p/SPL13-6 module responds to ABA, IAA, and ethylene and that SPL13-6 participates in the juvenile–adult phase transition. This research lays a foundation for further studies on regulation mechanisms involved in the juvenile–adult phase change in pear trees.

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Acknowledgements

This work was supported by the Doctoral Foundation of Shandong Province (ZR2019BC003), the Breeding Project of Shandong Province (2019LZGC008), and the China Agricultural Research System (CARS-29-07).

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  1. Minyan Song and Anqi Li have contributed equally to this work.

Authors and Affiliations

  1. College of Horticulture, Qingdao Key Lab of Genetic Improvement and Breeding of Horticultural Plants, Qingdao Agricultural University, Qingdao, 266109, China

    Minyan Song, Anqi Li, Lei Sun, Yuling Mei, Zhiyan Wang, Rihong Wang, Ran Wang, Dingli Li, Jiankun Song & Yingjie Yang

  2. Taishan Academy of Forestry Sciences, Tai’an, 271000, China

    Chunxiang Zhang

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  1. Minyan Song
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Contributions

MS, AL, and YY performed the experiments and wrote the article. LS, ZW, RW, and CZ helped with experiments. RW, JS, and DL modified the article.

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Correspondence to Yingjie Yang.

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Communicated by Heakeun Yun.

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Song, M., Li, A., Sun, L. et al. The miR156x + p/SPL13-6 module responds to ABA, IAA, and ethylene, and SPL13-6 participates in the juvenile–adult phase transition in Pyrus. Hortic. Environ. Biotechnol. 64, 437–448 (2023). https://doi.org/10.1007/s13580-022-00482-y

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