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Metacaspase MC1 enhances aluminum-induced programmed cell death of root tip cells in Peanut

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Abstract

Aims

Metacaspases are cysteine-dependent proteases, which play essential roles in programmed cell death (PCD), and caspase-3-like protease is the crucial executioner. However, its response mechanism to aluminum (Al)-induced PCD is still elusive.

Methods

Here, the type I metacaspase gene in peanut (Arachis hypoganea L.), AhMC1, was cloned from the Al-sensitive cultivar ZH2. Physiological and biochemical methods, as well as gene expression analyses, were employed to explore its function in Al-induced PCD in peanut root tips.

Results

AhMC1 had a 1068-bp open reading frame, encoding a peptide of 355 amino acids, and the purified protein exhibited a high caspase-3-like protease activity. Its expression levels in different tissues of peanut varieties ZH2 and 99–1507 (Al-tolerant) varied under Al-stress conditions. The subcellular localization indicated that AhMC1 was transferred from mitochondria into the cytoplasm. Furthermore, overexpressing AhMC1 reduced the resistance to Al stress. Sense transgenic plants showed a low relative root growth rate, and reduced superoxide dismutase, peroxidase, and catalase activities, compared with wild-type and antisense transgenic plants under Al-stress conditions, but had a high root-cell death rate, and increased Al and maleic dialdehyde contents.

Conclusions

The data suggest that metacaspase AhMC1 is a positive factor in Al-induced PCD in peanut root tips.

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Abbreviations

Al:

Aluminum

AT:

Antisense transgenic

CAT:

Catalase

MC:

Metacaspase

MDA:

Maleic dialdehyde

PCD:

Programmed cell death

POD:

Peroxidase

RACE:

Rapid amplification of cDNA ends

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

ST:

Sense transgenic

WT:

Wild-type

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31776190, 31560346, 31660350, 31701356, and 31860334), the Guangxi Natural Science Foundation of China (Grant No. 2016GXNSFBA380223), the Training Program for 1000 Young and Middle-aged Backbone Teachers of Guangxi Higher Education Institution in 2019.

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Author notes

  1. Shaochang Yao and Shuzhen Luo contributed equally to this work.

Authors and Affiliations

  1. College of Agronomy, Guangxi University, Nanning, Guangxi, China

    Shaochang Yao, Shuzhen Luo, Chunliu Pan, Weijiao Xiong, Dong Xiao, Aiqin Wang, Jie Zhan & Longfei He

  2. College of Pharmacy, Guangxi University of Chinese Medicine, Nanning, Guangxi, China

    Shaochang Yao

  3. College of Life Science and Technology, Guangxi University, Nanning, Guangxi, China

    Shaochang Yao & Chunliu Pan

  4. Guangxi Key Laboratory for Agro-Environment and Agro-Product Safety, Nanning, Guangxi, China

    Dong Xiao, Aiqin Wang, Jie Zhan & Longfei He

Authors
  1. Shaochang Yao
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  2. Shuzhen Luo
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  3. Chunliu Pan
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  4. Weijiao Xiong
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  5. Dong Xiao
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  7. Jie Zhan
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Contributions

JZ and LFH conceived the general strategy; SCY, LSZ and CLP performed the experiments and analyzed the data; SZL and DX interpreted the results; AQW and WJX cultured the seedlings for experiments; SCY and SZL wrote the manuscript. JZ revised the manuscript. All the authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jie Zhan or Longfei He.

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Yao, S., Luo, S., Pan, C. et al. Metacaspase MC1 enhances aluminum-induced programmed cell death of root tip cells in Peanut. Plant Soil 448, 479–494 (2020). https://doi.org/10.1007/s11104-020-04448-w

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