Skip to main content

Plant STAND P-loop NTPases: a current perspective of genome distribution, evolution, and function

Plant STAND P-loop NTPases: genomic organization, evolution, and molecular mechanism models contribute broadly to plant pathogen defense

Abstract

STAND P-loop NTPase is the common weapon used by plant and other organisms from all three kingdoms of life to defend themselves against pathogen invasion. The purpose of this study is to review comprehensively the latest finding of plant STAND P-loop NTPase related to their genomic distribution, evolution, and their mechanism of action. Earlier, the plant STAND P-loop NTPase known to be comprised of only NBS–LRRs/AP–ATPase/NB–ARC ATPase. However, recent finding suggests that genome of early green plants comprised of two types of STAND P-loop NTPases: (1) mammalian NACHT NTPases and (2) NBS–LRRs. Moreover, YchF (unconventional G protein and members of P-loop NTPase) subfamily has been reported to be exceptionally involved in biotic stress (in case of Oryza sativa), thereby a novel member of STAND P-loop NTPase in green plants. The lineage-specific expansion and genome duplication events are responsible for abundance of plant STAND P-loop NTPases; where “moderate tandem and low segmental duplication” trajectory followed in majority of plant species with few exception (equal contribution of tandem and segmental duplication). Since the past decades, systematic research is being investigated into NBS–LRR function supported the direct recognition of pathogen or pathogen effectors by the latest models proposed via ‘integrated decoy’ or ‘sensor domains’ model. Here, we integrate the recently published findings together with the previous literature on the genomic distribution, evolution, and distinct models proposed for functional molecular mechanism of plant STAND P-loop NTPases.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

ETI:

Effector-triggered immunity

HR:

Hypersensitive response

PRRs:

Pattern recognition receptors

PAMPs:

Pathogen-associated molecular patterns

PCD:

Programmed cell death

PTI:

PAMP triggered immunity

NACHT:

NAIP, C2TA, HET-E, and TP1

NB–ARC:

Nucleotide-binding site shared by APAF1, plant-resistance (R) genes, and CED-4

ROS:

Reactive oxygen species

STAND:

Signal transduction ATPases with numerous domains

References

  • Akita M, Valkonen JPT (2002) A novel gene family in moss (Physcomitrella patens) shows sequence homology and a phylogenetic relationship with the TIR-NBS class of plant disease resistance genes. J Mol Evol 55:595–605

    CAS  PubMed  Article  Google Scholar 

  • Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerström M (2006) Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J 47:947–959

    CAS  PubMed  Article  Google Scholar 

  • Arya P, Acharya V (2016) Computational identification raises a riddle for distribution of putative NACHT NTPases in the genome of early green plants. PLoS One 11:e0150634. doi:10.1371/journal.pone.0150634

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Arya P, Kumar G, Acharya V, Singh AK (2014) Genome-wide identification and expression analysis of NBS-encoding genes in Malus × domestica and expansion of NBS genes family in Rosaceae. PLoS One 9:e107987. doi:10.1371/journal.pone.0107987

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6:973–979

    CAS  PubMed  Article  Google Scholar 

  • Cannon SB, Zhu H, Baumgarten AM, Spangler R, May G, Cook DR, Young ND (2002) Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J Mol Evol 54:548–562

    CAS  PubMed  Article  Google Scholar 

  • Catanzariti AM, Dodds PN, Ve T, Kobe B, Ellis JG, Staskawicz BJ (2010) The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol Plant Microbe Interact 23:49–57

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y, Morel J-B, Fournier E, Tharreau D, Terauchi R, Kroj T (2013) The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25:1463–1481

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN (2014) A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front Plant Sci 5:606. doi:10.3389/fpls.2014.00606

    PubMed  PubMed Central  Article  Google Scholar 

  • Chen Y, Liu Z, Halterman DA (2012) Molecular determinants of resistance activation and suppression by phytophthora infestans effector IPI-O. PLoS Pathog 8(3):e1002595. doi:10.1371/journal.ppat.1002595

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cheng X, Jiang H, Zhao Y, Qian Y, Zhu S, Cheng B (2010) A genomic analysis of disease-resistance genes encoding nucleotide binding sites in Sorghum bicolor. Genet Mol Biol 33:292–297

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cheng Y, Li X, Jiang H, Ma W, Miao W, Yamada T, Zhang M (2012) Systematic analysis and comparison of nucleotide-binding site disease resistance genes in maize. FEBS J 279:2431–2443

    CAS  PubMed  Article  Google Scholar 

  • Cheung MY, Xue Y, Zhou L, Li MW, Sun SS, Lam HM (2010) An ancient P-loop GTPase in rice is regulated by a higher plant-specific regulatory protein. J Biol Chem 285:37359–37369

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Cheung MY, Li MW, Yung YL, Wen CQ, Lam HM (2013) The unconventional P-loop NTPase OsYchF1 and its regulator OsGAP1 play opposite roles in salinity stress tolerance. Plant Cell Environ 36:2008–2020

    CAS  PubMed  Google Scholar 

  • Cheung MY, Li X, Miao R, Fong YH, Li KP, Yung YL, Yu MH, Wong KB, Chen Z, Lam HM (2016) ATP binding by the P-loop NTPase OsYchF1 (an unconventional G protein) contributes to biotic but not abiotic stress responses. Proc Natl Acad Sci USA 113:2648–2653

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Christie N, Tobias PA, Naidoo S, Külheim C (2016) The Eucalyptus grandis NBS-LRR gene family: physical clustering and expression hotspots. Front Plant Sci 6:1238. doi:10.3389/fpls.2015.01238

    PubMed  PubMed Central  Article  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    CAS  PubMed  Article  Google Scholar 

  • Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci USA 100:8024–8029

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    CAS  PubMed  Article  Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103:8888–8893

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9(1):275–296

    Article  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman AR, Baker BJ (2007) The evolution of resistance genes in multi-protein plant resistance systems. Curr Opin Genet Dev 17:493–499

    CAS  PubMed  Article  Google Scholar 

  • Gassmann W, Hinsch ME, Staskawicz BJ (1999) The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20:265–277

    CAS  PubMed  Article  Google Scholar 

  • Guo YL, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D (2011) Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 157:757–769

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Gururani MA, Venkatesh J, Upadhyaya CP, Akula Nookaraju, Pandey SK, Park SW (2012) Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78:51–65

    CAS  Article  Google Scholar 

  • Holt BF, Boyes DC, Ellerström M, Siefers N, Wiig A, Kauffman S, Grant MR, Dangl JL (2002) An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev Cell 2:807–817

    PubMed  Article  Google Scholar 

  • Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527

    CAS  PubMed  Article  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312

    CAS  PubMed  Article  Google Scholar 

  • Igari K, Endo S, Hibara K, Aida M, Sakakibara H, Kawasaki T, Tasaka M (2008) Constitutive activation of a CC-NB-LRR protein alters morphogenesis through the cytokinin pathway in Arabidopsis. Plant J 55:14–27

    CAS  PubMed  Article  Google Scholar 

  • Inohara N, Chamaillard M, McDonald C, Nuñez G (2005) NOD-LRR PROTEINS: role in host–microbial interactions and inflammatory disease. Annu Rev Biochem 74:355–383

    CAS  PubMed  Article  Google Scholar 

  • Jacob F, Vernaldi S, Maekawa T (2013) Evolution and conservation of plant NLR functions. Front Immunol 4:297–316. doi:10.3389/fimmu.2013.00297

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–4014

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Jia Y, Yuan Y, Zhang Y, Yang S, Zhang X (2015) Extreme expansion of NBS-encoding genes in Rosaceae. BMC Genet 16:48. doi:10.1186/s12863-015-0208-x

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  PubMed  Article  Google Scholar 

  • Joshi RK, Nayak S (2013) Perspectives of genomic diversification and molecular recombination towards R-gene evolution in plants. Physiol Mol Biol Plants 19:1–9

    CAS  PubMed  Article  Google Scholar 

  • Joshi RK, Kar B, Nayak S (2011) Survey and characterization of NBS-LRR (R) genes in Curcuma longa transcriptome. Bioinformation 6:360–363

    PubMed  PubMed Central  Article  Google Scholar 

  • Jupe F, Pritchard L, Etherington GJ, Mackenzie K, Cock PJ, Wright F, Sharma SK, Bolser D, Bryan GJ, Jones JD, Hein I (2012) Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genom 13:75. doi:10.1186/1471-2164-13-75

    CAS  Article  Google Scholar 

  • Kang L, Li J, Zhao T, Xiao F, Tang X, Thilmony R, He SY, Zhou J-M (2003) Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci USA 100:3519–3524

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kang YJ, Kim KH, Shim S, Yoon MY, Sun S, Kim MY, Van K, Lee S-H (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol 12:139. doi:10.1186/1471-2229-12-139

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, Fournier E, Tharreau D, Terauchi R (2012) Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J 72:894–907

    CAS  PubMed  Article  Google Scholar 

  • Kim J, Lim CJ, Lee BW, Choi JP, Oh SK, Ahmad R, Kwon SY, Ahn J, Hur CG (2012) A genome-wide comparison of NB-LRR type of resistance gene analogs (RGA) in the plant kingdom. Mol Cells 33:385–392

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636

    CAS  PubMed  Article  Google Scholar 

  • Koonin EV, Aravind L (2000) The NACHT family—a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem Sci 25:223–224

    CAS  PubMed  Article  Google Scholar 

  • Krasileva KV, Dahlbeck D, Staskawicz BJ (2010) Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22:2444–2458

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kroj T, Chanclud E, Michel-Romiti C, Grand X, Morel JB (2016) Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytol 210:618–626

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kuang H, Woo S-S, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7:1195–1206

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317:41–72

    CAS  PubMed  Article  Google Scholar 

  • Leipe DD, Koonin EV, Aravind L (2004) STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 343:1–28

    CAS  PubMed  Article  Google Scholar 

  • Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20:116–122

    CAS  PubMed  Article  Google Scholar 

  • Li X, Cheng Y, Ma W, Zhao Y, Jiang H, Zhang M (2010) Identification and characterization of NBS-encoding disease resistance genes in Lotus japonicus. Plant Syst Evol 289:101–110

    Article  Google Scholar 

  • Lin X, Zhang Y, Kuang H, Chen J (2013) Frequent loss of lineages and deficient duplications accounted for low copy number of disease resistance genes in Cucurbitaceae. BMC Genom 14:335. doi:10.1186/1471-2164-14-335

    CAS  Article  Google Scholar 

  • Liu J-J, Ekramoddoullah AKM (2003) Isolation, genetic variation and expression of TIR-NBS-LRR resistance gene analogs from western white pine (Pinus monticola Dougl. ex. D. Don.). Mol Genet Genom 270:432–441

    CAS  Article  Google Scholar 

  • Liu S, Liu Y, Yang X et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930. doi:10.1038/ncomms4930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lozano R, Ponce O, Ramirez M, Mostajo N, Orjeda G (2012) Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS One 7:e34775. doi:10.1371/journal.pone.0034775

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Luo S, Zhang Y, Hu Q, Chen J, Li K, Lu C, Liu H, Wang W, Kuang H (2012) Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol 159:197–210

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lv S, Changwei Z, Tang J, Li Y, Wang Z, Jiang D, Hou X (2015) Genome-wide analysis and identification of TIR-NBS-LRR genes in Chinese cabbage (Brassica rapa ssp. pekinensis) reveal expression patterns to TuMV infection. Physiol Mol Plant Pathol 90:89–97

    CAS  Article  Google Scholar 

  • Malik S, Van der Hoorn RAL (2016) Inspirational decoys: a new hunt for effector targets. New Phytol 210:371–373

    PubMed  Article  Google Scholar 

  • Marone D, Russo MA, Laidò G, De Leonardis AM, Mastrangelo AM (2013) Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. Int J Mol Sci 14:7302–7326

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436

    CAS  PubMed  Article  Google Scholar 

  • McDowell JM, Simon SA (2006) Recent insights into R gene evolution. Mol Plant Pathol 7:437–448

    CAS  PubMed  Article  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332

    CAS  PubMed  Article  Google Scholar 

  • Meyers BC, Morgante M, Michelmore RW (2002) TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92

    CAS  PubMed  Article  Google Scholar 

  • Meyers B, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR—encoding genes in Arabidopsis. Plant Cell 15:809–834

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    CAS  PubMed  Article  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    CAS  PubMed  Article  Google Scholar 

  • Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447

    CAS  PubMed  Article  Google Scholar 

  • Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE, Staskawicz BJ, Rathjen JP (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18:2792–2806

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Mun JH, Yu HJ, Park S, Park BS (2009) Genome-wide identification of NBS-encoding resistance genes in Brassica rapa. Mol Genet Genom 282:617–631

    CAS  Article  Google Scholar 

  • Ntoukakis V, Balmuth AL, Mucyn TS, Gutierrez JR, Jones AM, Rathjen JP (2013) The tomato Prf complex is a molecular trap for bacterial effectors based on Pto transphosphorylation. PLoS Pathog 9:e1003123. doi:10.1371/journal.ppat.1003123

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M, Saitoh H, Fujibe T, Matsumura H, Shenton M, Galam DC, Undan J, Ito A, Sone T, Terauchi R (2011) A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J 66:467–479

    CAS  PubMed  Article  Google Scholar 

  • Pan Q, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213

    CAS  PubMed  Article  Google Scholar 

  • Papp B, Pál C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197

    CAS  PubMed  Article  Google Scholar 

  • Perazzolli M, Malacarne G, Baldo A, Righetti L, Bailey A, Fontana P, Velasco R, Malnoy M (2014) Characterization of resistance gene analogues (RGAs) in apple (Malus × domestica Borkh.) and their evolutionary history of the Rosaceae family. PLoS One 9:e83844. doi:10.1371/journal.pone.0083844

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Porter B, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ (2009) Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Genet Genom 281(6):609–626

    CAS  Article  Google Scholar 

  • Qian S, Wang Y, Ma H, Zhang L (2015) Expansion and functional divergence of jumonji C-containing histone demethylases: significance of duplications in ancestral angiosperms and vertebrates. Plant Physiol 168:1321–1337

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Rairdan G, Moffett P (2007) Brothers in arms? Common and contrasting themes in pathogen perception by plant NB-LRR and animal NACHT-LRR proteins. Microbes Infect 9:677–686

    CAS  PubMed  Article  Google Scholar 

  • Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19:76–84

    CAS  PubMed  Article  Google Scholar 

  • Salmeron JM, Barker SJ, Carland FM, Mehta AY, Staskawicz BJ (1994) Tomato mutants altered in bacterial disease resistance provide evidence for a new locus controlling pathogen recognition. Plant Cell 6:511–520

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV (2016) Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14:8. doi:10.1186/s12915-016-0228-7

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Savard L, Li P, Strauss SH, Chase MW, Michaud M, Bousquet J (1994) Chloroplast and nuclear gene sequences indicate late Pennsylvanian time for the last common ancestor of extant seed plants. Proc Natl Acad Sci USA 91:5163–5167

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Schornack S, Minsavage GV, Stall RE, Jones JB, Lahaye T (2008) Characterization of AvrHah1, a novel AvrBs3-like effector from Xanthomonas gardneri with virulence and avirulence activity. New Phytol 179:546–556

    CAS  PubMed  Article  Google Scholar 

  • Selin C, de Kievit TR, Belmonte MF, Fernando WGD (2016) Elucidating the role of effectors in plant–fungal interactions: progress and challenges. Front Microbiol 7:600. doi:10.3389/fmicb.2016.00600

    PubMed  PubMed Central  Article  Google Scholar 

  • Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, Chintha R, Harzen A, Colby T, Kamoun S, van der Hoorn RA (2008) Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 20:1169–1183

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–1233

    CAS  PubMed  Article  Google Scholar 

  • Shao ZQ, Zhang YM, Hang YY, Xue JY, Zhou GC, Wu P, Wu XY, Wu XZ, Wang Q, Wang B, Chen JQ (2014) Long-term evolution of nucleotide-binding site-leucine-rich repeat genes: understanding gained from and beyond the legume family. Plant Physiol 166:217–234

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Shao ZQ, Xue JY, Wu P, Zhang YM, Wu Y, Hang YY, Wang B, Chen JQ (2016) Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiol 170:2095–2109

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Tan S, Wu S (2012) Genome wide analysis of nucleotide-binding site disease resistance genes in Brachypodium distachyon. Comp Funct Genom 2012:418208. doi:10.1155/2012/418208

    Article  CAS  Google Scholar 

  • Tarr DEK, Alexander HM (2009) TIR-NBS-LRR genes are rare in monocots: evidence from diverse monocot orders. BMC Res Notes 2:197. doi:10.1186/1756-0500-2-197

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Ueda H, Yamaguchi Y, Sano H (2006) Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol Biol 61:31–45

    CAS  PubMed  Article  Google Scholar 

  • van der Biezen EA, Jones JD (1998a) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8:R226–R228

    PubMed  Article  Google Scholar 

  • van der Biezen EA, Jones JD (1998b) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456

    PubMed  Article  Google Scholar 

  • van der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • van Ooijen G, van den Burg HA, Cornelissen BJC, Takken FLW (2007) Structure and function of resistance proteins in Solanaceous plants. Annu Rev Phytopathol 45:43–72

    PubMed  Article  CAS  Google Scholar 

  • Wan H, Zhao Z, Malik AA, Qian C, Chen J (2010) Identification and characterization of potential NBS-encoding resistance genes and induction kinetics of a putative candidate gene associated with downy mildew resistance in Cucumis. BMC Plant Biol 10:186. doi:10.1186/1471-2229-10-186

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Wan H, Yuan W, Ye Q, Wang R, Ruan M, Li Z, Zhou G, Yao Z, Zhao J, Liu S, Yang Y (2012) Analysis of TIR- and non-TIR-NBS-LRR disease resistance gene analogous in pepper: characterization, genetic variation, functional divergence and expression patterns. BMC Genom 13:502. doi:10.1186/1471-2164-13-502

    CAS  Article  Google Scholar 

  • Wan H, Yuan W, Bo K, Shen J, Pang X, Chen J (2013) Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genom 14:109. doi:10.1186/1471-2164-14-109

    CAS  Article  Google Scholar 

  • Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115

    CAS  PubMed  Article  Google Scholar 

  • Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF, Segonzac C, Ve T, Ma Y, Saucet SB, Ericsson DJ, Casey LW, Lonhienne T, Winzor DJ, Zhang X, Coerdt A, Parker JE, Dodds PN, Kobe B, Jones JD (2014) Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344:299–303

    CAS  PubMed  Article  Google Scholar 

  • Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K, Dong S, Schornack S, Zipfel C, Robatzek S, Hogenhout SA, Kamoun S (2012) Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb Symp Quant Biol 77:235–247

    CAS  PubMed  Article  Google Scholar 

  • Wu C-H, Krasileva KV, Banfield MJ, Terauchi R, Kamoun S (2015) The “sensor domains” of plant NLR proteins: more than decoys? Front Plant Sci 6:134. doi:10.3389/fpls.2015.00134

    PubMed  PubMed Central  Google Scholar 

  • Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120

    CAS  PubMed  Article  Google Scholar 

  • Xue J-Y, Wang Y, Wu P, Wang Q, Yang LT, Pan XH, Wang B, Chen JQ (2012) A primary survey on bryophyte species reveals two novel classes of nucleotide-binding site (NBS) genes. PLoS One 7:e36700. doi:10.1371/journal.pone.0036700

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Yang S, Feng Z, Zhang X, Jiang K, Jin X, Hang Y, Chen JQ, Tian D (2006) Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 62:181–193

    CAS  PubMed  Article  Google Scholar 

  • Yang S, Zhang X, Yue JX, Tian D, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom 280:187–198

    CAS  Article  Google Scholar 

  • Young ND, Zhou P, Silverstein KA (2016) Exploring structural variants in environmentally sensitive gene families. Curr Opin Plant Biol 30:19–24

    CAS  PubMed  Article  Google Scholar 

  • Yu J, Tehrim S, Zhang F, Tong C, Huang J, Cheng X, Dong C, Zhou Y, Qin R, Hua W, Liu S (2014) Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana. BMC Genom 15:3. doi:10.1186/1471-2164-15-3

    Article  Google Scholar 

  • Yue JX, Meyers BC, Chen JQ, Tian D, Yang S (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol 193:1049–1063

    CAS  PubMed  Article  Google Scholar 

  • Zhai C, Zhang Y, Yao N, Lin F, Liu Z, Dong Z, Wang L, Pan Q (2014) Function and interaction of the coupled genes responsible for Pik-h encoded rice blast resistance. PLoS One 9:e98067. doi:10.1371/journal.pone.0098067

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zhang YM, Shao ZQ, Wang Q, Hang YY, Xue JY, Wang B, Chen JQ (2016) Uncovering the dynamic evolution of nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes in Brassicaceae. J Integr Plant Biol 58:165–177

    CAS  PubMed  Article  Google Scholar 

  • Zhou J-M, Chai J (2008) Plant pathogenic bacterial type III effectors subdue host responses. Curr Opin Microbiol 11:179–185

    PubMed  Article  CAS  Google Scholar 

  • Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genom 271:402–415

    CAS  Article  Google Scholar 

  • Zipfel C, Rathjen JP (2008) Plant immunity: AvrPto targets the frontline. Curr Biol 18:R218–R220

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

We are grateful to the Director, CSIR-Institute of Himalayan Bioresource Technology (CSIR-IHBT), Palampur, India for providing necessary facilities. PA gratefully acknowledges University Grant Commission (UGC), Government of India for providing fellowship. This work was financially supported by Council of Scientific and Industrial Research (CSIR), New Delhi, India in the form of CSIR network project “Computational Systems and Network Biology”. Authors are thankful to the Department of Biotechnology, Government of India for infrastructural support in the form of Bioinformatics Infrastructure Facility (BIF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. This manuscript represents CSIR-IHBT communication number: 3890.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vishal Acharya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by S. Hohmann.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arya, P., Acharya, V. Plant STAND P-loop NTPases: a current perspective of genome distribution, evolution, and function. Mol Genet Genomics 293, 17–31 (2018). https://doi.org/10.1007/s00438-017-1368-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-017-1368-3

Keywords

  • STAND P-loop NTPase
  • NACHT NTPase
  • Nucleotide-binding site–leucine-rich repeats (NBS–LRRs)
  • Evolution
  • Disease-resistance genes
  • Molecular mechanism