Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Biological function of nonxpressor of pathogenesis-related genes 1 (NPR1) in response to biotic and abiotic stresses

생물학 및 비생물학적 스트레스 반응에서의 NPR1 기능 고찰

  • Cheong, Mi Sun (Division of Applied Life Science (BK21plus program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University) ;
  • Kim, Sewon (Advanced Radiation Technology Institute (ARTI), Korea Atomic Energy Research Institute (KAERI)) ;
  • Yun, Dae-Jin (Division of Applied Life Science (BK21plus program), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University)
  • 정미선 (경상대학교 대학원 응용생명과학부, 식물생명공학연구소) ;
  • 김세원 (한국원자력연구원 첨단방사선연구소) ;
  • 윤대진 (경상대학교 대학원 응용생명과학부, 식물생명공학연구소)
  • Received : 2016.05.10
  • Accepted : 2016.08.05
  • Published : 2016.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Plants can recognize and respond in various ways to diverse environmental stresses, including pathogenic microorganisms, salt, drought, and low temperature. Salicylic acid (SA) is one phytohormone that plays important roles in the regulation of plant growth and development. Nonexpressor of pathogenesis-related genes 1 (NPR1) was originally identified as a core protein that could function as a transcriptional co-regulator and SA receptor during systemic acquired resistance (SAR), a plant immune response that could activate PR genes after pre-exposure of a pathogen. Although the function of NPR1 in plant defense response and the role of SA hormone in the regulation of plant physiological processes have been well characterized, the biological role of NPR1 in plant abiotic stress responses is largely unknown. In this review, we will summarize and discuss the current understanding of NPR1 function in response to plant environmental stresses.

Keywords

References

  1. Alavi SMN, Arvin MJ, Kalantari KM (2014). Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticum aestivum L.) seedlings. J. Plant Interac. 9:683-688 https://doi.org/10.1080/17429145.2014.900120
  2. Bandurska H, Stroinski A (2005) The effect of salicylic acid on barley response to water deficit. Acta Physiol. Plant 27:379-386 https://doi.org/10.1007/s11738-005-0015-5
  3. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol. 126:1024-1030 https://doi.org/10.1104/pp.126.3.1024
  4. Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. Plant Cell 6:1583-1592 https://doi.org/10.1105/tpc.6.11.1583
  5. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57-63 https://doi.org/10.1016/S0092-8674(00)81858-9
  6. Cao Y, Zhang ZW, Xue L W, Du JB, Shang J, Xu F, Yuan S, Lin HH (2009) Lack of salicylic acid in Arabidopsis protects plants against moderate salt stress. Z. Naturforsch. C 64:231-238
  7. Cecchini NM, Monteoliva MI, Alvarez ME (2011) Proline dehydrogenase contributes to pathogen defense in Arabidopsis. Plant Physiol. 155:1947-1959 https://doi.org/10.1104/pp.110.167163
  8. Chen J, Zhu C, Li L P, Sun Z Y (2007) Effects of exogenous salicylic acid on growth and H2O2- metabolizing enzymes in rice seedlings under lead stress. J. Environ. Sci. 19:44-49 https://doi.org/10.1016/S1001-0742(07)60007-2
  9. Cheong MS, Yun DJ (2007) Salt-stress signaling. J Plant Biol. 50:148-155 https://doi.org/10.1007/BF03030623
  10. Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005) Overexpression of a riceNPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol. Plant-Microbe Interact. 18:511-520 https://doi.org/10.1094/MPMI-18-0511
  11. Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J. 27:101-113 https://doi.org/10.1046/j.1365-313x.2001.01070.x
  12. Chi YH, Paeng SK, Kim MJ, Hwang GY, Melencion SM, Oh HT, Lee SY (2013) Redox-dependent functional switching of plant proteins accompanying with their structural changes. Front Plant Sci 4:277
  13. Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong XN (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12:2175-2190 https://doi.org/10.1105/tpc.12.11.2175
  14. Clarke SM. Mur LA, Wood JE. Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thanliana. Plant J. 38:432-447 https://doi.org/10.1111/j.1365-313X.2004.02054.x
  15. DalCorso G, Manara A, Piasentin S, Furini A (2014) Nutrient metal elements in plants. Metallomics. 6:1770-1788 https://doi.org/10.1039/C4MT00173G
  16. Delaney TP, Friedrich L, Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. 92:6602-6606 https://doi.org/10.1073/pnas.92.14.6602
  17. Ding Y, Dommal M, Mou Z (2016) Avscisic acid promotes proteosome-mediated degrdadation of the transcription coactivator NPR1 in Arabidopsis thaliana. Plant J. 86:20-34 https://doi.org/10.1111/tpj.13141
  18. Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol. 10:151 https://doi.org/10.1186/1471-2229-10-151
  19. Dong FC, Wang PT, Song CP (2001) The role of hydrogen peroxide ub salicylic acid-induced stomatal closure in Vicia fava guard cells. Plant Cell 21:972-984
  20. Drazic G, Mihailovic N (2005) Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Sci 168:511-517 https://doi.org/10.1016/j.plantsci.2004.09.019
  21. Fan W, Dong X (2002) In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14:1377-1389 https://doi.org/10.1105/tpc.001628
  22. Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, Dong X (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228-232 https://doi.org/10.1038/nature11162
  23. Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutant with enhanced disease susceptibility by directing screening. Genetics 143:973-982
  24. Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812-818 https://doi.org/10.1126/science.1185383
  25. Han Y, Chaouch S, Mhamdi A, Queval G, Zechmann B, Notor G (2013) Functional analysis of Arabidopsis mutants points to novel roles for glutathione in coupleing H(2)O(2) to activation of salicylic acid accumulation and signaling. Antioxid Redox Signal 18:2016-2021 https://doi.org/10.1089/ars.2013.1506
  26. Horvath E, Pal M, Szalai G, Paldi E, and Janda T (2007). Exogenous 4- hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. Biol. Plant. 51:480-487 https://doi.org/10.1007/s10535-007-0101-1
  27. Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: A balancing act to optimize fitness. Mol. Plant 7:1267-1287 https://doi.org/10.1093/mp/ssu049
  28. Janda T, Szalai G, Tari I, Paldi E (1999) Hydrophonic treatment with salicylic acid decrease the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175-180 https://doi.org/10.1007/s004250050547
  29. Jayakannan M, Bose J, Babourina O, Shabala S, Massart A, Poschenrieder C, Rengel Z (2015) The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J Exp Bot. 66:1865-1875 https://doi.org/10.1093/jxb/eru528
  30. Kang GZ, Wang ZX, Sun GC (2003) Participation of H2O2 in enhancement of cold chilling by salicylic acid in banana seedlings. Acta Bot Sin 45:567-573
  31. Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571-576 https://doi.org/10.1034/j.1399-3054.2002.1150411.x
  32. Khan MIR, Asgher M, Khan NA (2014). Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol. Biochem. 80:67-74 https://doi.org/10.1016/j.plaphy.2014.03.026
  33. Khan MIR, Iqbal N, Masood A, Per S, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal. Behav. 8:e26374 https://doi.org/10.4161/psb.26374
  34. Kong J, Dong Y, Xu L, Liu S, Bai X (2014) Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. Bot. Stud. 55:9 https://doi.org/10.1186/1999-3110-55-9
  35. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CM (2008) Kinetics of salicylatemediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147:1358-1368 https://doi.org/10.1104/pp.108.121392
  36. Kovacs Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol. 208:860-872 https://doi.org/10.1111/nph.13502
  37. Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J. Plant Physiol. 165: 920-931 https://doi.org/10.1016/j.jplph.2006.11.014
  38. Lee SY, Damodaran PN, Roh KS (2014). Influence of salicylic acid on rubisco and rubisco activase in tobacco plant grown under sodium chloride in vitro. Saudi J. Biol. Sci. 21:417-426 https://doi.org/10.1016/j.sjbs.2014.04.002
  39. Li G, Peng X, Wei L, Kang G (2013) Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 529:321-325 https://doi.org/10.1016/j.gene.2013.07.093
  40. Lindermayr C, Sell S, Muller B, Leister D, Durner J (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894-2907 https://doi.org/10.1105/tpc.109.066464
  41. Loutfy N, El-Tayeb MA, Hassanen AM, Moustafa MF, Sakuma Y, Inouhe M (2012) Changes in the water status and osmotic solute contents in response to drought and salicylic acid treatments in four different cultivars of wheat (Triticum aestivum). J Plant Res. 125:173-84 https://doi.org/10.1007/s10265-011-0419-9
  42. Madan P, Jagadish SV, Craufurd PQ, Fitzgerald M, Lafarge T, Wheeler TR (2012) Effect of elevated CO2 and high temperature on seed-set and grain quality of rice. J Exp Bot. 63:3843-3852 https://doi.org/10.1093/jxb/ers077
  43. Matika and Loake (2014) Redox regulation in plant immune function Antioxid. Redox. Signal 21:1373-1388 https://doi.org/10.1089/ars.2013.5679
  44. Mishra S, Heckathorn SA, Barua D, Wang D, Joshi P, Hamilton Iii EW, Frantz J (2008) Interactive effects of elevated Co2 and ozone on leaf thermotolerance in field-grown Glycine max. J Integr Plant Biol. 50:1396-1405 https://doi.org/10.1111/j.1744-7909.2008.00745.x
  45. Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J. 73:91-104 https://doi.org/10.1111/tpj.12014
  46. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935-944 https://doi.org/10.1016/S0092-8674(03)00429-X
  47. Okuma E, Nozawa R, Murata Y, Miura K (2014) Plant Signal Behav. 9:e28085 https://doi.org/10.4161/psb.28085
  48. Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS (2013) Tell me more: roles of NPRs in plant immunity. Trends Plant Sci 18:402-411 https://doi.org/10.1016/j.tplants.2013.04.004
  49. Pawlak-Sprada S, Arasimowicz-Jelonek M, Podgorska M, and Deckert J (2011). Activation of phenylpropanoid pathway in legume plants exposed to heavy metals. Part I. Effects of cadmium and lead on phenylalanine ammonialyase gene expression, enzyme activity and lignin content. Acta Biochim. Pol. 58, 211-216
  50. Potters G. Horemans N. Jansen MAK (2010) The cellular redox state in plant stress biology-a charging concept. Plant Physiol. Biochem. 48:292-300 https://doi.org/10.1016/j.plaphy.2009.12.007
  51. Quilis J, Penas G, Messeguer J, Brugidou C, San Segundo B (2008) The Arabidopsis AtNPR1 inversely modulates defense response against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol Plant Microbe Interact. 21:1215-1231 https://doi.org/10.1094/MPMI-21-9-1215
  52. Ray DK, Gerber JS, MacDonald GK, and West PC (2015) Climate variation explains a third of global crop yield variablility Nature Comm. 5989; doi:10.1038/ncomms6989
  53. Rusterucci C, Espunya MC, Diaz M, Chabannes M, Martinez MC (2007) S-nitrosoglutathion reductase affords protection against pathogens in Arabdiopsis, both locally and systemically. Plant Physiol. 143:1282-1292 https://doi.org/10.1104/pp.106.091686
  54. Saleh A, Withers J, Mohan R, Marques J, Gu Y, Yan S, Zavaliev R, Nomoto M, Tada Y, Dong X (2015) Posttranslational modification of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host Microbe. 18:169-182 https://doi.org/10.1016/j.chom.2015.07.005
  55. Sandhu D, Tasma IM, Frasch R, Bhattacharyya MK (2009) Systemic acquired resistance in soybean is regulsted by two proteins, orthologous to Arabidopsis NPR1. BMC Plant Biol. 9:105 https://doi.org/10.1186/1471-2229-9-105
  56. Saruhan N, Saglam A, Kadioglu A (2012) Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiol Plant. 34:97-106 https://doi.org/10.1007/s11738-011-0808-7
  57. Scott IM, Clarke SM, Wood JE, Mur LA (2004) Salycilate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol. 135:1040-1049 https://doi.org/10.1104/pp.104.041293
  58. Shah J, Tsui F, Klessig DF (1997) Characterization of a salicylic acid-insenitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact. 10:69-78 https://doi.org/10.1094/MPMI.1997.10.1.69
  59. Shi Q, bao Z, SZhu Z, Ying Q, Qian Q (2006) Effects of different treatmetns of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul. 48:127-135 https://doi.org/10.1007/s10725-005-5482-6
  60. Shi Z, Maximova S, Liu Y, Verica J, Guiltinan MJ (2013) The salicylic acid receptor NPR3 is a negative regulator of the transcriptional defense response during early flower development in Arabidopsis. Mol. Plant 6:802-816 https://doi.org/10.1093/mp/sss091
  61. Siboza XI, Bertling I, Odindo AO (2014). Salicylic acid and methyl jasmonate improve chilling tolerance in cold-stored lemon fruit (Citrus limon). J. Plant Physiol. 171: 1722-1731 https://doi.org/10.1016/j.jplph.2014.05.012
  62. Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot. 115:433-47 https://doi.org/10.1093/aob/mcu239
  63. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860-872 https://doi.org/10.1016/j.cell.2009.03.038
  64. Srinivasan T, Raja Rajesh Kumar K, Meur G, Kirti PB (2009) Heterologous expression of Arabidopsis NPR1 (AtNPR1) enhances oxidative stress tolerance in transgenic tobacco plants. Biotechnol Lett 31:1343-1351 https://doi.org/10.1007/s10529-009-0022-5
  65. Stevens J, Senaratna T, Sivasithamparam K (2006) Salicylic acid induces salinity tolerance in tomato (Lycopersicon esculentum cv. Roma): associated changes in gas exchange, water relations and membrane stabilisation. Plant Growth Regul 49:77-83
  66. Strobel NE, Kuc A (1995) Chemical and biological inducers of systemic acquired resistance to pathogens protect cucumber and tobacco from damage caused by paraquat and cupric chloride. Phytopathology 85:1306-1310 https://doi.org/10.1094/Phyto-85-1306
  67. Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic stress and biotic stress combination. New Phytol. 203:32-43 https://doi.org/10.1111/nph.12797
  68. Szalai G, Krantev A, Yordanova R, Popova L P, Janda T (2013) Influence of salicylic acid on phytochelatin synthesis in Zea mays during Cd stress. Turk. J. Bot. 37: 708-714
  69. Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952-956 https://doi.org/10.1126/science.1156970
  70. Tester M, and Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818-822 https://doi.org/10.1126/science.1183700
  71. Volko SM, Boller T, Ausubel FM (1998) Isolation of new Arabidopsis mutants with enhanced disease susceptibility to Pseduomonas syringae by direct screening. Genetics 149:537-548
  72. Wildermuth M C, Dewdney J, Wu G, Ausubel F M (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562-565 https://doi.org/10.1038/35107108
  73. Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang M, Li Q, Yang D, He Z (2007) Functional analysis of rce NPR1-like gene reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 5:313-324 https://doi.org/10.1111/j.1467-7652.2007.00243.x
  74. Zhang JY, Qia YS, Lv D, Gao ZH, Qu SC, , Zhang Z (2012) Malus hupehensis NPR1 induces pathogenesis-related protein gene expression in transgenic tobacco. Plant Biol. 14:46-56 https://doi.org/10.1111/j.1438-8677.2011.00483.x
  75. Zhang JY, Qu SC, Qia YS, Zhang Z, Guo ZR (2014) Overexpression of the Malus hupenhensis MhNPR1 gene increased tolerance to salt and osmotic stress in transgenic tobacco. Mol Biol Rep 41:1553-1561 https://doi.org/10.1007/s11033-013-3001-9
  76. Zhang Y, He Q, Zhao S, Huang L, Hao L (2014) Arabidopsis ein2-1 and npr1-1 response to Al stress. Bull Environ Contam Toxicol. 93:78-83 https://doi.org/10.1007/s00128-014-1249-y
  77. Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252: 911-924 https://doi.org/10.1007/s00709-014-0732-y
  78. Zhong X, Xi L, Lian Q, Luo X, Wu Z, Seng S, Yuan X, Yi M (2015) The NPR1 homolog GhNPR1 plays an important role in the defense response of Gladiolus hybridus. Plant Cell Rep. 34:1063-1074 https://doi.org/10.1007/s00299-015-1765-1