Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

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

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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

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

References

  1. Abbink TEM, Peart JR, Mos TNM, Baulcombe DC, Bol JF, Linthorst HJM (2002) Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants. Virology 295:307–319

  2. Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H et al (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:74–178

  3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

  4. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

  5. Beyer A (1997) Sequence analysis of the AAA protein family. Protein Sci 6:2043–2058

  6. Buaboocha T, Liao B, Zielinski RE (2001) Isolation of cDNA and genomic DNA clones encoding a calmodulin-binding protein related to a family of ATPases involved in cell division and vesicle fusion. Planta 212:774–781

  7. Bussemer J, Chigri F, Vothknecht UC (2009) Arabidopsis ATPase family gene 1-like protein 1 is a calmodulin-binding AAA+-ATPase with a dual localization in chloroplasts and mitochondria. FEBS J 276:3870–3880

  8. Dangl JL, Dietrich RA, Richberg MH (1996) Death don’t have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8:1793–1807

  9. Dereeper A, Guignon V, Blanc G, Audic S, Buffer S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469

  10. Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL (1994) Arabidopsis mutants simulating disease resistance response. Cell 77:565–577

  11. Falk A, Feys B, Frost LN, Jones JDG, Daniels MJ, Parker JE (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci USA 96:3292–3297

  12. Feng BH, Yang Y, Shi YF, Shen HC, Wang HM, Huang QN, Xu X, Lü XG, Wu JL (2013) Characterization and genetic analysis of a novel rice spotted-leaf mutant HM47 with broad-spectrum resistance to Xanthomonas oryzae pv. oryzae. J Integr Plant Biol 55:473–483

  13. Genoud T, Buchala AJ, Chua N-H, Métraux J-P (2002) Phytochrome signaling modulates the SA-perceptive pathway in Arabidopsis. Plant J 31:87–95

  14. Glazebrook J, Zook M, Mert F, Kagan I, Rogers EE, Crute IR, Holub EB, Hammerschmidt R, Ausubel FM (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146:381–392

  15. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626–629

  16. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312

  17. Greenberg JT, Ailan G, Klessig DF, Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551–563

  18. Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defenses. Plant Cell 8:1773–1791

  19. Heath MC (2000) Hypersensitive response-related death. Plant Mol Bil 44:321–334

  20. Jian-yang M, Sun-lu C, Jian-hui Z, Yan-jun D, Sheng T (2012) Identification and genetic mapping of a lesion mimic mutant in rice. Rice Sci 19:1–7

  21. Johal GS, Hulbert SH, Briggs SP (1995) Disease lesion mimics of maize—a model for cell-death in plants. Bioassays 17:685–692

  22. Kanzaki H, Nirasawa S, Saitoh H, Ito M, Nishihara M, Terauchi R, Nakamura I (2002) Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor Appl Genet 105:809–814

  23. Kinoshita CT (1995) Report of committee on gene symbolization, nomenclature and linkage groups. Rice Genet News 12:9–115

  24. Kiyosawa S (1970) Inheritance of a particular sensitivity of the rice variety, Sekiguchi Asahi, to pathogens and chemicals and linkage relationship with blast resistance. Bull Nat Inst Agric Sci 21:61–71

  25. Kunau WH, Beyer A, Franken T, Gotte K, Marzioch M, Saidowsky J, Skaletz-Rorowski A, Wiebel FF (1993) Two complementary approaches to study peroxisome biogenesis in Saccharomyces cerevisiae: forward and reversed genetics. Biochimie 75:209–224

  26. Liu G, Wang L, Zhou Z, Leung H, Wang GL, He C (2004) Physical mapping of a rice lesion mimic gene, Spl1, to a 70 kb segment of rice chromosome 12. Mol Genet Genom 272:108–115

  27. Matin MN, Pandeya D, Baek KH, Lee DS, Lee JH, Kang HD, Kang SG (2010) Phenotypic and genotypic analysis of rice lesion mimic mutants. Plant Pathol J 26(2):159–169

  28. Midoh N, Iwata M (1996) Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol 37:9–18

  29. Midoh N, Iwata M (1997) Expression of defense-related genes by probenazole or 1,2-benzisothiazole-3 (2H)-one 1,1-dioxide. J Pesticide Sci 22:45–47

  30. Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45:445–450

  31. Mittler R, Rizhsky L (2000) Transgene-induced lesion mimic. Plant Mol Biol 44:335–344

  32. Mizobuchi R, Hirabayashi H, Kaiji R, Nishizawa Y, Yoshimura A, Satoh H, Ogawa T, Okamoto M (2002) Isolation and characterization of rice lesion-mimic mutants with enhanced resistance to rice and bacterial blight. Plant Sci 163:345–353

  33. Mizobuchi K, Hirabayashi H, Kaji R, Nishizawa Y, Satoh H, Ogawa T, Okamoto M (2003) Developmental responses of resistance to Magnaporthe grisea and Xanthomonas campestris pv. oryzae in lesion-mimic mutants of rice. Breed Sci 53:93–100

  34. Moeder W, Yoshioka K (2008) Lesion mimic mutants. A classical, yet still fundamental approach to study programmed cell death. Plant Signal Behav 10:764–767

  35. Mori M, Tomita C, Sugimoto K, Hasegawa M, Hayashi N, Dubouzet JG, Ochiai H, Sekimoto H, Hirochika H, Kikuchi S (2007) Isolation and molecular characterization of a spotted leaf 18 mutant by modified activation tagging in rice. Plant Mol Biol 63:847–860

  36. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8:4321–4325

  37. Nagao S, Takahashi M, Morimura K (1964) Genetical studies on rice plant: XXVIII. Causal genes and their linkage relationships of some morphological characters introduced from foreign rice varieties. Mem Fac Agric Hokkaido Univ 5(2):89–96

  38. Ogura T, Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6:575–597

  39. Patel S, Latterich M (1998) The AAA team: related ATPases with diverse functions. Trends Cell Biol 8:65–71

  40. Qiao Y, Jiang W, Lee JH, Park BS, Cho MS, Piao R, Woo MO, Roh JH, Han L, Paek NC, Seo HS, Koh HJ (2010) An SPL28 gene encoding clathrin-associated adaptor protein complex 1 medium subunit l1 (AP1M1) is responsible for spotted leaf and early senescence in rice (Oryza sativa L.). New Phytol 185:258–274

  41. Rakshit S, Kanzaki K, Matsumura H, Rakshit A, Fujibe T, Okuyama Y, Yoshida K, Tamiru M, Shenton M, Utsushi H, Mitsuoka M, Abe A, Kiuchi Y, Terauch Y (2010) Use of TILLING for reverse and forward genetics of rice. In: Meksem K, Kahl G (eds) The handbook of plant mutation screening: mining of natural and induced alleles. Wiley, Weinheim, pp 187–197

  42. Sekiguchi Y, Furuta T (1965) On a rice mutant showing particular reaction to some spotting disease. Preliminary report. Ann Phytopathol Soc Jpn 30:71–72 (in Japanese)

  43. Sugimoto M, Yamaguchi Y, Nakamura K, Tatsumi Y, Sano H (2004) A hypersensitive response-induced ATPase associated with various cellular activities (AAA) protein from tobacco plants. Plant Mol Biol 56:973–985

  44. Sun CH, Liu LC, Tang JY, Lin A, Zhang F, Fang J, Zhang G, Chu C (2011) RLIN1, encoding a putative coproporphyrinogen III oxidase, is involved in lesion initiation in rice. J Genet Genomics 38:29–37

  45. Takahashi A, Kawasaki T, Henmi K, Shil K, Kodama O, Satoh H, Shimamoto K (1999) Lesion mimic mutants of rice with alterations in early signaling events of defense. Plant J 17:535–545

  46. Takahashi A, Agrawal GK, Yamazaki M, Onosato K, Miyao A, Kawasaki T, Shimamota K, Hirochika H (2007) Rice Pti1a negatively regulates RAR1-dependent defense responses. Plant Cell 19:2940–2951

  47. Takahashi Y, Berberich T, Kanzaki H, Matsumura H, Saitoh H, Kusano T, Terauchi R (2009) Serine palmitoyltransferase, the first step enzyme in sphingolipid biosynthesis, is involved in nonhost resistance. Mol Plant Microbe Interact 22:31–38

  48. Terauchi R, Abe A, Takagi H, Yoshida K, Kosugi S, Natsume S, Yaegashi H, Kanzaki H, Matsumura H, Mitsuoka C, Utsushi H, Tamiru M (2012) Whole geneome sequencing and future breeding of rice. J Plant Biochem Biotechnol 12:S10–S14

  49. Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976

  50. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403

  51. Undan JR, Tamiru M, Abe A, Yoshida K, Kosugi S, Takagi H, Yoshida K, Kanzaki H, Saitoh H, Fekih R, Sharma S, Undan J, Yano M, Terauchi R (2012) Mutation in OsLMS, a gene encoding a protein with two double stranded RNA binding motifs, causes lesion mimic phenotype and early senescence in rice (Oryza sativa L.). Genes Genet Syst 87:169–179

  52. Urantowka A, Knorpp C, Olczak T, Kolodziejczak M, Janska H (2005) Plant mitochondria contain at least two i-AAA-like complexes. Plant Mol Biol 59:239–252

  53. van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

  54. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949–956

  55. Wang L, Pei Z, Tian Y, He C (2005) OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation. Mol Plant Microbe Interact 18(5):375–384

  56. White SR, Lauring B (2007) AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 8:1657–1667

  57. Wu C, Bordeos A, Madamba MRZ, Baraoidan M, Ramos M, Wang G, Leach JA, Leung H (2008) Rice lesion mimic mutants with enhanced resistance to diseases. Mol Genet Genomics 279:605–619

  58. Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci USA 99:7530–7535

  59. Yin Z, Chen J, Zeng L, Goh M, Leung H, Khush GS, Wang G (2000) Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13:869–876

  60. Zeng LR, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang GL (2004) Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16:2795–2808

Download references

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.

Author information

Correspondence to Muluneh Tamiru.

Additional information

Communicated by S. Hohmann.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • ATPase
  • Defense response
  • Lesion mimic
  • Cell death
  • Oryza sativa