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A mutation in a coproporphyrinogen III oxidase gene confers growth inhibition, enhanced powdery mildew resistance and powdery mildew-induced cell death in Arabidopsis

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Abstract

Key message

A gene encoding a coproporphyrinogen III oxidase mediates disease resistance in plants by the salicylic acid pathway.

Abstract

A number of genes that regulate powdery mildew resistance have been identified in Arabidopsis, such as ENHANCED DISEASE RESISTANCE 1 to 3 (EDR1 to 3). To further study the molecular interactions between the powdery mildew pathogen and Arabidopsis, we isolated and characterized a mutant that exhibited enhanced resistance to powdery mildew. The mutant also showed dramatic powdery mildew-induced cell death as well as growth defects and early senescence in the absence of pathogens. We identified the affected gene by map-based cloning and found that the gene encodes a coproporphyrinogen III oxidase, a key enzyme in the tetrapyrrole biosynthesis pathway, previously known as LESION INITIATION 2 (LIN2). Therefore, we designated the mutant lin2-2. Further studies revealed that the lin2-2 mutant also displayed enhanced resistance to Hyaloperonospora arabidopsidis (H.a.) Noco2. Genetic analysis showed that the lin2-2-mediated disease resistance and spontaneous cell death were dependent on PHYTOALEXIN DEFICIENT 4 (PAD4), SALICYLIC ACID INDUCTION-DEFICIENT 2 (SID2), and NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1), which are all involved in salicylic acid signaling. Furthermore, the relative expression levels of defense-related genes were induced after powdery mildew infection in the lin2-2 mutant. These data indicated that LIN2 plays an important role in cell death control and defense responses in plants.

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Abbreviations

LIN2:

LESION INITIATION 2

CPO:

Coproporphyrinogen III oxidase

EDR1:

ENHANCED DISEASE RESISTANCE 1

PAD4:

PHYTOALEXIN DEFICIENT 4

SID2:

SALICYLIC ACID INDUCTION-DEFICIENT 2

NPR1:

NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1

EIN2:

ETHYLENE INSENSITIVE 2

COI1:

CORONATINE-INSENSITIVE 1

KEG:

KEEP ON GOING

SR1:

SIGNAL RESPONSIVE1

LMMs:

Lesion mimic mutants

PCD:

Programmed cell death

SA:

Salicylic acid

JA:

Jasmonic acid

ET:

Ethylene

HR:

Hypersensitive response

SAR:

Systemic acquired resistance

DAB:

Diaminobenzidine

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Acknowledgments

This study was financially supported by the National Transgenic Program of China (Grant No. 2011ZX08005-002) and by the National Transgenic Program of China (Grant No. 2009ZX08009-036B).

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  1. College of Life Science, Shihezi University, Shihezi, 832003, Xinjiang, People’s Republic of China

    Chuan-yu Guo, Jin Xing, Wen-qi Li & Bai-ming Cui

  2. State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China

    Guang-heng Wu & Ding-zhong Tang

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  1. Chuan-yu Guo
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  2. Guang-heng Wu
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  3. Jin Xing
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Correspondence to Ding-zhong Tang or Bai-ming Cui.

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Communicated by Y. Lu.

C. Guo and G. Wu contributed equally to this work.

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Guo, Cy., Wu, Gh., Xing, J. et al. A mutation in a coproporphyrinogen III oxidase gene confers growth inhibition, enhanced powdery mildew resistance and powdery mildew-induced cell death in Arabidopsis. Plant Cell Rep 32, 687–702 (2013). https://doi.org/10.1007/s00299-013-1403-8

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  • DOI: https://doi.org/10.1007/s00299-013-1403-8

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