Cell autonomous and non-autonomous functions of plant intracellular immune receptors in stomatal defense and apoplastic defense

English version

Autoři: Jiapei Yan ^aff001; Huiyun Yu ^aff001; Bo Li ^aff003; Anqi Fan ^aff001; Jeffrey Melkonian ^aff005; Xiue Wang ^aff004; Tong Zhou ^aff002; Jian Hua ^aff001
Působiště autorů: School of Integrative Plant Science, Plant Biology Section, Cornell University, Ithaca, NY, United States of America ^aff001; Key Laboratory of Food Quality and Safety, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China ^aff002; School of Applied Physics and Engineering, Cornell University, Ithaca, NY, United States of America ^aff003; State Key Lab of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, China ^aff004; School of Integrative Plant Science, Crop and Soil Sciences, Cornell University, Ithaca, NY, United States of America ^aff005
Vyšlo v časopise: Cell autonomous and non-autonomous functions of plant intracellular immune receptors in stomatal defense and apoplastic defense. PLoS Pathog 15(10): e32767. doi:10.1371/journal.ppat.1008094
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1008094

Souhrn

Stomatal closure defense and apoplastic defense are two major immunity mechanisms restricting the entry and propagation of microbe pathogens in plants. Surprisingly, activation of plant intracellular immune receptor NLR genes, while enhancing whole plant disease resistance, were sometimes linked to a defective stomatal defense in autoimmune mutants. Here we report the use of high temperature and genetic chimera to investigate the inter-dependence of stomatal and apoplastic defenses in autoimmunity. High temperature inhibits both stomatal and apoplastic defenses in the wild type, and it suppresses constitutive apoplastic defense responses and rescues the deficiency of stomatal closure response in autoimmune mutants. Chimeric plants have been generated to activate NLR only in guard cells or the non-guard cells. NLR activation in guard cells inhibits stomatal closure defense response in a cell autonomous manner likely through repressing ABA responses. At the same time, it leads to increased whole plant resistance accompanied by a slight increase in apoplastic defense. In addition, NLR activation in both guard and non-guard cells affects stomatal aperture and water potential. This study thus reveals that NLR activation has a differential effect on immunity in a cell type specific matter, which adds another layer of immune regulation with spatial information.

Klíčová slova:

Gene expression – Plant pathogens – Genetically modified plants – Leaves – Stomata – Guard cells – Mesophyll cells – Plant disease resistance

Zdroje

1. Sawinski K, Mersmann S, Robatzek S, Bohmer M (2013) Guarding the green: pathways to stomatal immunity. Mol Plant Microbe Interact 26: 626–632. doi: 10.1094/MPMI-12-12-0288-CR 23441577

2. Zeng W, He SY (2010) A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153: 1188–1198. doi: 10.1104/pp.110.157016 20457804

3. Melotto M, Zhang L, Oblessuc PR, He SY (2017) Stomatal Defense a Decade Later. Plant Physiol 174: 561–571. doi: 10.1104/pp.16.01853 28341769

4. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969–980. doi: 10.1016/j.cell.2006.06.054 16959575

5. Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nature immunology 6: 973. doi: 10.1038/ni1253 16177805

6. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803–814. doi: 10.1016/j.cell.2006.02.008 16497589

7. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323–329. doi: 10.1038/nature05286 17108957

8. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual review of plant biology 60: 379–406. doi: 10.1146/annurev.arplant.57.032905.105346 19400727

9. Böhm H, Albert I, Fan L, Reinhard A, Nürnberger T (2014) Immune receptor complexes at the plant cell surface. Current Opinion in Plant Biology 20: 47–54. doi: 10.1016/j.pbi.2014.04.007 24835204

10. McLachlan DH, Kopischke M, Robatzek S (2014) Gate control: guard cell regulation by microbial stress. New Phytol 203: 1049–1063. doi: 10.1111/nph.12916 25040778

11. Doehlemann G, Hemetsberger C (2013) Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol 198: 1001–1016. doi: 10.1111/nph.12277 23594392

12. Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Current opinion in plant biology 15: 349–357. doi: 10.1016/j.pbi.2012.05.006 22705024

13. Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66: 487–511. doi: 10.1146/annurev-arplant-050213-040012 25494461

14. Asai S, Shirasu K (2015) Plant cells under siege: plant immune system versus pathogen effectors. Curr Opin Plant Biol 28: 1–8. doi: 10.1016/j.pbi.2015.08.008 26343014

15. Su J, Zhang M, Zhang L, Sun T, Liu Y, et al. (2017) Regulation of Stomatal Immunity by Interdependent Functions of a Pathogen-Responsive MPK3/MPK6 Cascade and Abscisic Acid. Plant Cell 29: 526–542. doi: 10.1105/tpc.16.00577 28254778

16. Zeng W, Brutus A, Kremer JM, Withers JC, Gao X, et al. (2011) A genetic screen reveals Arabidopsis stomatal and/or apoplastic defenses against Pseudomonas syringae pv. tomato DC3000. PLoS pathogens 7: e1002291. doi: 10.1371/journal.ppat.1002291 21998587

17. Mang HG, Qian W, Zhu Y, Qian J, Kang HG, et al. (2012) Abscisic acid deficiency antagonizes high-temperature inhibition of disease resistance through enhancing nuclear accumulation of resistance proteins SNC1 and RPS4 in Arabidopsis. Plant Cell 24: 1271–1284. doi: 10.1105/tpc.112.096198 22454454

18. Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14: 310–317. doi: 10.1016/j.tplants.2009.03.006 19443266

19. Zhang Y, Goritschnig S, Dong X, Li X (2003) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. The Plant Cell 15: 2636–2646. doi: 10.1105/tpc.015842 14576290

20. Kim TH, Hauser F, Ha T, Xue S, Bohmer M, et al. (2011) Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway. Curr Biol 21: 990–997. doi: 10.1016/j.cub.2011.04.045 21620700

21. Yang DL, Shi Z, Bao Y, Yan J, Yang Z, et al. (2017) Calcium Pumps and Interacting BON1 Protein Modulate Calcium Signature, Stomatal Closure, and Plant Immunity. Plant Physiol 175: 424–437. doi: 10.1104/pp.17.00495 28701352

22. Yang S, Hua J (2004) A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell 16: 1060–1071. doi: 10.1105/tpc.020479 15031411

23. Gou M, Zhang Z, Zhang N, Huang Q, Monaghan J, et al. (2015) Opposing Effects on Two Phases of Defense Responses from Concerted Actions of HEAT SHOCK COGNATE70 and BONZAI1 in Arabidopsis. Plant Physiol 169: 2304–2323. doi: 10.1104/pp.15.00970 26408532

24. Cheng C, Gao X, Feng B, Sheen J, Shan L, et al. (2013) Plant immune response to pathogens differs with changing temperatures. Nat Commun 4: 2530. doi: 10.1038/ncomms3530 24067909

25. Huot B, Castroverde CDM, Velasquez AC, Hubbard E, Pulman JA, et al. (2017) Dual impact of elevated temperature on plant defence and bacterial virulence in Arabidopsis. Nat Commun 8: 1808. doi: 10.1038/s41467-017-01674-2 29180698

26. Hua J (2013) Modulation of plant immunity by light, circadian rhythm, and temperature. Curr Opin Plant Biol 16: 406–413. doi: 10.1016/j.pbi.2013.06.017 23856082

27. Alcazar R, Parker JE (2011) The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci 16: 666–675. doi: 10.1016/j.tplants.2011.09.001 21963982

28. Murdock CC, Paaijmans KP, Bell AS, King JG, Hillyer JF, et al. (2012) Complex effects of temperature on mosquito immune function. Proc Biol Sci 279: 3357–3366. doi: 10.1098/rspb.2012.0638 22593107

29. Hua J (2014) Temperature and plant immunity. Temperature and Plant Development: Wiley Blackwell Publisher. pp. 163–180.

30. Wang Y, Bao Z, Zhu Y, Hua J (2009) Analysis of temperature modulation of plant defense against biotrophic microbes. Mol Plant Microbe Interact 22: 498–506. doi: 10.1094/MPMI-22-5-0498 19348568

31. Zhu Y, Qian W, Hua J (2010) Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog 6: e1000844. doi: 10.1371/journal.ppat.1000844 20368979

32. Kim YS, An C, Park S, Gilmour SJ, Wang L, et al. (2017) CAMTA-Mediated Regulation of Salicylic Acid Immunity Pathway Genes in Arabidopsis Exposed to Low Temperature and Pathogen Infection. Plant Cell 29: 2465–2477. doi: 10.1105/tpc.16.00865 28982964

33. Yang Y, Costa A, Leonhardt N, Siegel RS, Schroeder JI (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4: 6. doi: 10.1186/1746-4811-4-6 18284694

34. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469. doi: 10.1104/pp.103.027979 14555774

35. Liu XY, Sun YL, Korner CJ, Du XR, Vollmer ME, et al. (2015) Bacterial Leaf Infiltration Assay for Fine Characterization of Plant Defense Responses using the Arabidopsis thaliana-Pseudomonas syringae Pathosystem. Jove-Journal of Visualized Experiments.

36. Yu H, Yan J, Du X, Hua J (2018) Overlapping and differential roles of plasma membrane calcium ATPases in Arabidopsis growth and environmental responses. Journal of experimental botany 69: 2693–2703. doi: 10.1093/jxb/ery073 29506225

37. Bauer H, Ache P, Lautner S, Fromm J, Hartung W, et al. (2013) The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Current Biology 23: 53–57. doi: 10.1016/j.cub.2012.11.022 23219726

38. Yoo S-D, Cho Y-H, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature protocols 2: 1565. doi: 10.1038/nprot.2007.199 17585298

39. Campbell GS (1985) Soil physics with BASIC: transport models for soil-plant systems. Amsterdam; New York: Elsevier. xvi, 150 p. p.

40. Khokon AR, Okuma E, Hossain MA, Munemasa S, Uraji M, et al. (2011) Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environ 34: 434–443. doi: 10.1111/j.1365-3040.2010.02253.x 21062318

41. Boursiac Y, Lee SM, Romanowsky SM, Blank RR, Sladek C, et al. (2010) Disruption of the vacuolar calcium-ATPases in Arabidopsis results in the activation of a salicylic acid-dependent programmed cell death pathway. Plant physiology: pp. 110.159038.

42. Wright CA, Beattie GA (2004) Pseudomonas syringae pv. tomato cells encounter inhibitory levels of water stress during the hypersensitive response of Arabidopsis thaliana. Proc Natl Acad Sci U S A 101: 3269–3274. doi: 10.1073/pnas.0400461101 14981249

43. Mantyla E, Lang V, Palva ET (1995) Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LT178 and RAB18 proteins in Arabidopsis thaliana. Plant physiology 107: 141–148. doi: 10.1104/pp.107.1.141 12228349

44. Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, et al. (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol 7: e1000139. doi: 10.1371/journal.pbio.1000139 19564897

45. Wang Z, Meng P, Zhang X, Ren D, Yang S (2011) BON1 interacts with the protein kinases BIR1 and BAK1 in modulation of temperature-dependent plant growth and cell death in Arabidopsis. Plant J 67: 1081–1093. doi: 10.1111/j.1365-313X.2011.04659.x 21623975

46. Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci U S A 99: 16314–16318. doi: 10.1073/pnas.252461999 12446847

47. Prodhan MY, Munemasa S, Nahar MN-E-N, Nakamura Y, Murata Y (2018) Guard cell salicylic acid signaling is integrated into abscisic acid signaling via the Ca2+/CPK-dependent pathway. Plant physiology: pp. 00321.02018.

48. Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27: 64–70. doi: 10.1105/tpc.114.133090 25604442