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The rice (Oryza sativa L.) LESION MIMIC RESEMBLING, which encodes an AAA-type ATPase, is implicated in defense response

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Abstract

Lesion mimic mutants (LMMs) provide a useful tool to study defense-related programmed cell death (PCD) in plants. Although a number of LMMs have been identified in multiple species, most of the candidate genes are yet to be isolated. Here, we report the identification and characterization of a novel rice (Oryza sativa L.) lesion mimic resembling (lmr) mutant, and cloning of the corresponding LMR gene. The LMR locus was initially delineated to 1.2 Mb region on chromosome 6, which was further narrowed down to 155-kb using insertions/deletions (INDELs) and cleavage amplified polymorphic sequence markers developed in this study. We sequenced the open reading frames predicted within the candidate genomic region, and identified a G–A base substitution causing a premature translation termination in a gene that encodes an ATPase associated with various cellular activities type (AAA-type) protein. RNA interference transgenic lines with reduced LMR transcripts exhibited the lesion mimic phenotype similar to that of lmr plants. Furthermore, expression of the wild-type LMR in the mutant background complemented the lesion phenotype, confirming that the mutation identified in LMR is responsible for the mutant phenotype. The pathogenesis-related (PR) genes PBZ1 and PR1 were induced in lmr, which also showed enhanced resistance to rice blast (Magnaporthe oryzae) and bacterial blight (Xanthomonas oryzae pv. oryzae), suggesting LMR is a negative regulator of cell death in rice. The identification of lmr and cloning of the corresponding LMR gene provide an additional resource for the study of PCD in plants.

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Abbreviations

CAPS:

Cleavage amplified polymorphic sequence

DAB:

Diamino benzidine

EMS:

Ethyl methanesulfonate

HR:

Hypersensitive response

INDELs:

Insertions and deletions

LMR:

Lesion mimic resembling

PR:

Pathogenesis related

PCD:

Programmed cell death

RT-PCR:

Reverse transcription polymerase chain reaction

SSR:

Simple sequence repeat

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Acknowledgments

This project was partially supported by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry, Grant-in-aid for MEXT (Scientific Research on Innovative Areas 23113009), and JSPS KAKENHI (Grant No. 24248004) to RT. RF is a postdoctoral fellow of the Japanese Society for the Promotion of Sciences (JSPS). We thank D. Baulcombe of Sainsbury Laboratory, John Innes Center, for providing us the 35S-p19 vector.

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Authors and Affiliations

  1. Iwate Biotechnology Research Center, Narita 22-174-4, Kitakami, Iwate, 024-0003, Japan

    Rym Fekih, Muluneh Tamiru, Hiroyuki Kanzaki, Akira Abe, Kentaro Yoshida, Eiko Kanzaki, Hiromasa Saitoh, Hiroki Takagi, Satoshi Natsume, Jerwin R. Undan, Jesusa Undan & Ryohei Terauchi

  2. Iwate Agricultural Research Center, Narita 20-1, Kitakami, Iwate, 024-0003, Japan

    Akira Abe

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  1. Rym Fekih
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  2. Muluneh Tamiru
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  3. Hiroyuki Kanzaki
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  4. Akira Abe
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  5. Kentaro Yoshida
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Correspondence to Muluneh Tamiru.

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Communicated by S. Hohmann.

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Fekih, R., Tamiru, M., Kanzaki, H. et al. The rice (Oryza sativa L.) LESION MIMIC RESEMBLING, which encodes an AAA-type ATPase, is implicated in defense response. Mol Genet Genomics 290, 611–622 (2015). https://doi.org/10.1007/s00438-014-0944-z

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