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Enhanced SA and Ca2+ signaling results in PCD-mediated spontaneous leaf necrosis in wheat mutant wsl

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Abstract

Leaf is the major photosynthesis organ and the key source of wheat (Triticum aestivum L.) grain. Spotted leaf (spl) mutant is a kind of leaf lesion mimic mutants (LMMs) in plants, which is an ideal material for studying the mechanisms of leaf development. In this study, we report the leaf abnormal development molecular mechanism of a spl mutant named white stripe leaf (wsl) derived from wheat cultivar Guomai 301 (WT). Histochemical observation indicated that the leaf mesophyll cells of the wsl were destroyed in the necrosis regions. To explore the molecular regulatory network of the leaf development in mutant wsl, we employed transcriptome analysis, histochemistry, quantitative real-time PCR (qRT-PCR), and observations of the key metabolites and photosynthesis parameters. Compared to WT, the expressions of the chlorophyll synthesis and photosynthesis-related homeotic genes were repressed; many genes in the WRKY transcription factor (TF) families were highly expressed; the salicylic acid (SA) and Ca2+ signal transductions were enhanced in wsl. Both the chlorophyll contents and the photosynthesis rate were lower in wsl. The contents of SA and reactive oxygen species (ROS) were significantly higher, and the leaf rust resistance was enhanced in wsl. Based on the experimental data, a primary molecular regulatory model for leaf development in wsl was established. The results indicated that the SA accumulation and enhanced Ca2+ signaling led to programmed cell death (PCD), and ultimately resulted in spontaneous leaf necrosis of wsl. These results laid a solid foundation for further research on the molecular mechanism of leaf development in wheat.

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Data availability

Raw sequencing data presented in this paper are available under the NCBI Sequence Read Archive (SRA) accession number PRJNA704463.

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Acknowledgements

We are grateful for the assistance by Shangqiu Academy of Agricultural and Forestry Sciences.

Funding

This study was supported by the Science and Technology Project in Henan Province (No. 212102110060) and National Key Research and Development Program ‘Science and Technology Innovation of High Grain Production Efficiency’ of China (No. 2018YFD0300701).

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Contributions

HL and ZJ contributed equally to this work. HL and ZJ performed all the experiments and analyzed the data. PZ, TW, JZ, JL and ZY helped with sowing and sample preparation. YN and YJ selected the mutant. XY and LL contributed to the field experiments and maintenance of the wheat accessions. JN and DH designed the whole study and drafted the manuscript and gave the final approval to the version of the manuscript that is being sent for consideration for publication.

Corresponding authors

Correspondence to Jishan Niu or Dexian He.

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The authors declare there are no competing interests.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Communicated by Stefan Hohmann.

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Li, H., Jiao, Z., Zhang, P. et al. Enhanced SA and Ca2+ signaling results in PCD-mediated spontaneous leaf necrosis in wheat mutant wsl. Mol Genet Genomics 296, 1249–1262 (2021). https://doi.org/10.1007/s00438-021-01811-z

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  • DOI: https://doi.org/10.1007/s00438-021-01811-z

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