Monodehydroascorbate reductase gene, regulated by the wheat PN-2013 miRNA, contributes to adult wheat plant resistance to stripe rust through ROS metabolism

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 1, 2014, Pages 1-12

  Feng, Hao ^a   Wang, Xiaojie ^a   Zhang, Qiong ^a   Fu, Yanping ^a   Feng, Chuanxin ^a   Wang, Bing ^a   Huang, Lili ^a   Kang, Zhensheng ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Adult plant resistance; MiRNA; Monodehydroascorbate reductase; Puccinia striiformis f. sp. tritici; ROS; Wheat

Indexed keywords

DEHYDROASCORBIC ACID REDUCTASE; HYDROGEN PEROXIDE; MESSENGER RNA; MICRORNA; MONODEHYDROASCORBATE REDUCTASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; LEAF GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT LEAF; PRIORITY JOURNAL; REPORTER GENE; RNA CLEAVAGE; SEEDLING; STABLE EXPRESSION; STRIPE RUST; TOBACCO; WHEAT;

ADULT PLANT RESISTANCE; APR; APX; ASA-GSH CYCLE; ASCORBATE PEROXIDASE; ASCORBATE-GLUTATHIONE CYCLE; CAT; CATALASE; CHINESE YELLOW RUST 32; CYR32; DAYS POST VIRUS INOCULATION; DEHYDROASCORBATE REDUCTASE; DHAR; DPVI; HOURS POST INOCULATION; HPI; MDHAR; MICRORNA; MIRNA; MONODEHYDROASCORBATE REDUCTASE; PCD; PROGRAMMED CELL DEATH; PUCCINIA STRIIFORMIS F. SP. TRITICI; QRT-PCR; QUANTITATIVE REAL TIME POLYMERASE CHAIN REACTION; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROS; RT-PCR; SOD; SUPEROXIDE DISMUTASE; VIGS; VIRUS INDUCED GENE SILENCE; WHEAT; XINGZI 9104; XZ;

BASIDIOMYCOTA; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; MICRORNAS; NADH, NADPH OXIDOREDUCTASES; PLANT DISEASES; PLANT LEAVES; REACTIVE OXYGEN SPECIES; SEEDLING; TRITICUM;

EID: 84890071599     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.11.001     Document Type: Article

References (55)

1. Chen X.M. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Can. J. Plant Pathol. 2005, 27:314-337.
2. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 2010, 11:539-548.
3. Thrall P.H., Burdon J.J. Evolution of virulence in a plant host-pathogen metapopulation. Science 2003, 299:1735-1737.
4. Line Roland F Virulence, Aggressiveness, Evolution, and Distribution of Races of Puccinia striiformis (the Cause of Stripe Rust of Wheat) in North America, 1968-87 1992, U.S. Dept. of Agriculture, Agricultural Research Service; National Technical Information Service, [Washington, D.C.] : Springfield, VA (5285 Port Royal Rd., Springfield 22161).
5. Sawhney R.N., Sharma J.B., Sharma D.N. Genetic diversity for adult plant resistance to leaf rust (Puccinia recondita) in near-isogenic lines and in Indian wheats. Plant Breed. 1992, 109:248-254.
6. Singh R.P. Genetic association of leaf rust resistance gene Lr34 with adult plant resistance to stripe rust in bread wheat. Phytopathology 1992, 82:835-838.
7. McIntosh R.A. Close genetic linkage of genes conferring adult-plant resistance to leaf rust and stripe rust in wheat. Plant Pathol. 1992, 41:523-527.
8. Liu H.M., Liu T.G., Xu S.C., Liu D.Q., Chen W.Q. Inheritance of yellow rust resistance in an elite wheat germplasm Xingzi 9104. Acta Agron. Sin. 2006, 32:1742-1745.
9. Zhang H., Wang C., Cheng Y., Chen X., Han Q., Huang L., Wei G., Kang Z. Histological and cytological characterization of adult plant resistance to wheat stripe rust. Plant Cell Rep. 2012, 31:2121-2137.
10. Huang X.L., Ma J.B., Chen X., Wang X.J., Ding K., Han D.J., Qu Z.P., Huang L.L., Kang Z.S. Genes involved in adult plant resistance to stripe rust in wheat cultivar Xingzi 9104. Physiol. Mol. Plant Pathol. 2013, 81:26-32.
11. Bolwell G.P. Role of active oxygen species and NO in plant defence responses. Curr. Opin. Plant Biol. 1999, 2:287-294.
12. 2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiol. Mol. Plant Pathol. 2007, 71:230-239.
13. Noctor G., Foyer C.H. ASCORBATE AND GLUTATHIONE: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49:249-279.
14. Nakano Y., Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981, 22:867-880.
15. Arrigoni O., Dipierro S., Borraccino G. Ascorbate free radical reductase, a key enzyme of the ascorbic acid system. FEBS Lett. 1981, 125:242-244.
16. Mittova V., Volokita M., Guy M., Tal M. Activities of SOD and the ascorbate-glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiol. Plant. 2000, 110:42-51.
17. Polle A., Schwanz P., Rudolf C. Developmental and seasonal changes of stress responsiveness in beech leaves (Fagus sylvatica L.). Plant Cell Environ. 2001, 24:821-829.
18. Leterrier M., Corpas F.J., Barroso J.B., Sandalio L.M., del Río L.A. Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol. 2005, 138:2111-2123.
19. Stevens R., Page D., Gouble B., Garchery C., Zamir D., Causse M. Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ. 2008, 31:1086-1096.
20. Navarro L., Dunoyer P., Jay F., Arnold B., Dharmasiri N., Estelle M., Voinnet O., Jones J.D.G. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312:436-439.
21. Zhang X., Zhao H., Gao S., Wang W.C., Katiyar Agarwal S., Huang H.D., Raikhel N., Jin H. Arabidopsis argonaute 2 regulates innate immunity via miRNA393*-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol. Cell 2011, 42:356-366.
22. Jagadeeswaran G., Saini A., Sunkar R. Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 2009, 229:1009-1014.
23. Zhu C., Ding Y., Liu H. MiR398 and plant stress responses. Physiol. Plant. 2011, 143:1-9.
24. Rogers S., Bendich A. Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol. Biol. 1985, 5:69-76.
25. Feng H., Huang X., Zhang Q., Wei G., Wang X., Kang Z. Selection of suitable inner reference genes for relative quantification expression of microRNA in wheat. Plant Physiol. Biochem. 2012, 51:116-122.
26. Jefferson R.A., Kavanagh T.A., Bevan M.W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 1987, 6:3901-3907.
27. -δδCT method. Methods 2001, 25:402-408.
28. Holzberg S., Brosio P., Gross C., Pogue G.P. Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J. 2002, 30:315-327.
29. Wang X., Tang C., Zhang H., Xu J.R., Liu B., Lv J., Han D., Huang L., Kang Z. TaDAD2, a negative regulator of programmed cell death, is important for the interaction between wheat and the stripe rust fungus. Mol. Plant Microbe Interact. 2011, 24:79-90.
30. Hou W.C., Liu J.S., Chen H.J., Chen T.E., Chang C.F., Lin Y.H. Dioscorin, the major tuber storage protein of yam (Dioscorea batatas decne) with carbonic anhydrase and trypsin inhibitor activities. J. Agric. Food Chem. 1999, 47:2168-2172.
31. Erkan M., Wang S.Y., Wang C.Y. Effect of UV treatment on antioxidant capacity, antioxidant enzyme activity and decay in strawberry fruit. Postharvest Biol. Tecnol. 2008, 48:163-171.
32. Yao Y., Guo G., Ni Z., Sunkar R., Du J., Zhu J.K., Sun Q. Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol. 2007, 8:R96.
33. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
34. Aukerman M.J., Sakai H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 2003, 15:2730-2741.
35. Jin H. Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett. 2008, 582:2679-2684.
36. Katiyar-Agarwal S., Jin H. Role of small RNAs in host-microbe interactions. Annu. Rev. Phytopathol. 2010, 48:225-246.
37. Dat J., Vandenabeele S., Vranova E., Van Montagu M., Inze D., Van Breusegem F. Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 2000, 57:779-795.
38. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 1997, 11:1187-1194.
39. Torres M.A., Jones J.D.G., Dangl J.L. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 2006, 141:373-378.
40. Nikovics K., Blein T., Peaucelle A., Ishida T., Morin H., Aida M., Laufs P. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 2006, 18:2929-2945.
41. Adam H., Marguerettaz M., Qadri R., Adroher B., Richaud F., Collin M., Thuillet A.C., Vigouroux Y., Laufs P., Tregear J.W., Jouannic S. Divergent expression patterns of miR164 and CUP-SHAPED COTYLEDON genes in palms and other monocots: implication for the evolution of meristem function in angiosperms. Mol. Biol. Evol. 2011, 28:1439-1454.
42. Kaneko T., Katoh T., Sato S., Nakamura A., Asamizu E., Tabata S. Structural analysis of Arabidopsis thaliana chromosome 3. II. Sequence features of the 4,251,695bp regions covered by 90 P1, TAC and BAC clones. DNA Res. 2000, 7:217-221.
43. Lisenbee C.S., Lingard M.J., Trelease R.N. Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J. 2005, 43:900-914.
44. Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004, 9:490-498.
45. Mittler R., Herr E.H., Orvar B.L., van Camp W., Willekens H., Inze D., Ellis B.E. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl. Acad. Sci. 1999, 96:14165-14170.
46. Solomon M., Belenghi B., Delledonne M., Menachem E., Levine A. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 1999, 11:431-444.
47. Peng M., Kuc J. Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks. Phytopathology 1992, 82:696-699.
48. Tenhaken R., Rubel C. Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol. 1997, 115:291-298.
49. Tenhaken R., Levine A., Brisson L.F., Dixon R.A., Lamb C. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. 1995, 92:4158-4163.
50. Barth C., Moeder W., Klessig D.F., Conklin P.L. The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol. 2004, 134:1784-1792.
51. Pavet V., Olmos E., Kiddle G., Mowla S., Kumar S., Antoniw J., Alvarez M.E., Foyer C.H. Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol. 2005, 139:1291-1303.
52. Asselbergh B., Curvers K., França S.C., Audenaert K., Vuylsteke M., Van Breusegem F., Höfte M. Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol. 2007, 144:1863-1877.
53. 2 generation and metabolism in leaf apoplastic fraction of tomato leaves infected with Botrytis cinerea. J. Phytopathol. 2003, 151:153-161.
54. Pastori G.M., Kiddle G., Antoniw J., Bernard S., Veljovic-Jovanovic S., Verrier P.J., Noctor G., Foyer C.H. Leaf vitamin C contents modulate plant defense transcripts and regulate genes that control development through hormone signaling. Plant Cell 2003, 15:939-951.
55. Colville L., Smirnoff N. Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants. J. Exp. Bot. 2008, 59:3857-3868.