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Identification and analysis of a differentially expressed wheat RING-type E3 ligase in spike primordia development during post-vernalization

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Abstract

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We identified a RING-type E3 ligase (TaBAH1) protein in winter wheat that targets TaSAHH1 for degradation and might be involved in primordia development by regulating targeted protein degradation.

Abstract

Grain yield per spike in wheat (Triticum aestivum), is mainly determined prior to flowering during mature primordia development; however, the genes involved in primordia development have yet to be characterized. In this study, we demonstrated that, after vernalization for 50 days at 4 °C, there was a rapid acceleration in primordia development to the mature stages in the winter wheat cultivars Keumgang and Yeongkwang compared with the Chinese Spring cultivar. Although Yeongkwang flowers later than Keumgang under normal condition, it has the same heading time and reaches the WS9 stage of floral development after vernalization for 50 days. Using RNA sequencing, we identified candidate genes associated with primordia development in cvs. Keumgang and Yeongkwang, that are differentially expressed during wheat reproductive stages. Among these, the RING-type E3 ligase TaBAH1 (TraesCS5B01G373000) was transcriptionally upregulated between the double-ridge (WS2.5) stage and later stages of floret primordia development (WS10) after vernalization. Transient expression analysis indicated that TaBAH1 was localized to the plasma membrane and nucleus and was characterized by self-ubiquitination activity. Furthermore, we found that TaBAH1 interacts with TaSAHH1 to mediate its polyubiquitination and degradation through a 26S proteasomal pathway. Collectively, the findings of this study indicate that TaBAH1 might play a prominent role in post-vernalization floret primordia development.

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Funding

This work was supported by a Korea University Grant and Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science, ICT & Future Planning (2017R1D1A1B06030349).

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Authors and Affiliations

  1. Department of Plant Biotechnology, Korea University, Seongbuk-Gu, Seoul, 02841, Republic of Korea

    Jae Ho Kim, Irfan Ullah Khan, Cheol Won Lee, Dae Yeon Kim & Yong Weon Seo

  2. Plant Genomics Laboratory, Department of Applied Plant Sciences, Kangwon National University, Chuncheon, 200-713, Republic of Korea

    Cheol Seong Jang, Sung Don Lim, Yong Chan Park & Ju Hee Kim

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  1. Jae Ho Kim
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Contributions

JHK, IUK, CWL, DYK, and YWS conceived and designed the experiments; JHK, IUK, CWL, YCP, JHK, and SDL performed the experiments; and JHK, IUK, DYK, and YWS analyzed the data and wrote the paper. All authors reviewed and approved the final manuscript.

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Supplementary Fig. S1.

qRT-PCR profiles of TaBAH1 induced by vernalization for 50 days in Chinese Spring, with the TaActin gene used as a control to normalize expression levels. Data represent the mean ± SD (n = 3) of three replicates (JPG 48 KB)

Supplementary Fig. S2.

qRT-PCR profiles of TaSAHH1 induced by vernalization for 50 days, with the TaActin gene used as a control to normalize expression levels. Data represent the mean ± SD (n = 3) of three replicates (JPG 93 KB)

Supplementary Fig. S3.

A 35S::TaSAHH1-GFP protein was transiently expressed in wheat protoplasts, and localization of the protein was scored (JPG 75 KB)

Supplementary Fig. S4. Specific UBCs provide evidence for the auto-ubiquitination of TaBAH1 in vitro

. (A) Multiple alignment among RING domain of BAH1 proteins. (B) Recombinant MBP-BAH1, MBP-BAH1 (C288A), His-UBC1, His-UBC2, His-UBC8, His-UBC9, His-UBC10, His-UBC11, and His-UBC19 proteins were purified from Escherichia coli extracts and used to assay MBP-BAH1 and MBP-BAH1 (C288A) for E3 activity in the presence of human E1, Arabidopsis UBCs, and ubiquitin. Polyubiquitinated TaBAH1 was detected using a Ubi antibody. C288A: MBP-TaBAH1 (C288A). (JPG 127 KB)

Supplementary Table S1.

The PCR primers used in this study. (XLSX 13 KB)

Supplementary Table S2.

Proteins that interact with TaBAH1 identified from a yeast two-hybrid screen. (XLSX 8 KB)

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Kim, J.H., Khan, I.U., Lee, C.W. et al. Identification and analysis of a differentially expressed wheat RING-type E3 ligase in spike primordia development during post-vernalization. Plant Cell Rep 40, 543–558 (2021). https://doi.org/10.1007/s00299-020-02651-8

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