Overexpression of a soybean salicylic acid methyltransferase gene confers resistance to soybean cyst nematode

Plant Biotechnology Journal

Volumn 11, Issue 9, 2013, Pages 1135-1145

  Lin, Jingyu ^a   Mazarei, Mitra ^a   Zhao, Nan ^a,d   Zhu, Junwei J ^b   Zhuang, Xiaofeng ^a   Liu, Wusheng ^a   Pantalone, Vincent R ^a   Arelli, Prakash R ^c   Stewart, Charles N ^a   Chen, Feng ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

^b USDA Agricultural Research Service Lincoln Nebraska   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

Heterodera glycines; Methyl salicylate; Soybean; Transgenic hairy roots

Indexed keywords

ESCHERICHIA COLI; GLYCINE MAX; HETERODERA GLYCINES;

COMPLEMENTARY DNA; METHYLTRANSFERASE; SALICYLIC ACID; SALICYLIC ACID METHYL ESTER; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; DISEASE RESISTANCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; HETERODERA GLYCINES; IMMUNOLOGY; KINETICS; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; PLANT ROOT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SOYBEAN; TRANSGENIC HAIRY ROOTS; TRANSGENIC PLANT; TYLENCHOIDEA;

HETERODERA GLYCINES; METHYL SALICYLATE; SOYBEAN; TRANSGENIC HAIRY ROOTS;

AMINO ACID SEQUENCE; ANIMALS; DISEASE RESISTANCE; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; KINETICS; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SALICYLIC ACID; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SOYBEANS; TYLENCHOIDEA;

EID: 84888136842     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12108     Document Type: Article

References (53)

1. Alieva, N.O., Konzen, K.A., Field, S.F., Meleshkevitch, E.A., Hunt, M.E., Beltran-Ramirez, V., Miller, D.J., Wiedenmann, J., Salih, A. and Matz, M.V. (2008) Diversity and evolution of coral fluorescent proteins. PLoS ONE, 3, e2680.
2. Alkharouf, N.W., Klink, V.P., Chouikha, I.B., Beard, H.S., MacDonald, M.H., Meyer, S., Knap, H.T., Khan, R. and Matthews, B.F. (2006) Timecourse microarray analyses reveal global changes in gene expression of susceptible Glycine max (soybean) roots during infection by Heterodera glycines (soybean cyst nematode). Planta, 224, 838-852.
3. Arelli, P.R., Sleper, D.A., Yue, P. and Wilcox, J.A. (2000) Soybean reaction to races 1 and 2 of Heterodera glycines. Crop Sci. 40, 824-826.
4. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 7, 248-254.
5. Byrd, D., Kirkpatrick, T. and Barker, K. (1983) An improved technique for clearing and staining plant tissue for detection of nematodes. J. Nematol. 15, 142-143.
6. Caldwell, B.E., Brim, C.A. and Ross, J.P. (1960) Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines. Agron. J. 52, 635-636.
7. Chen, H., Nelson, R.S. and Sherwood, J.L. (1994) Enhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection. Biotechniques, 16, 664-670.
8. Chen, F., D'Auria, J.C., Tholl, D., Ross, J.R., Gershenzon, J., Noel, J.P. and Pichersky, E. (2003a) An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 36, 577-588.
9. Chen, F., Tholl, D., D'Auria, J.C., Farooq, A., Pichersky, E. and Gershenzon, J. (2003b) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell, 15, 481-494.
10. Cook, D.E., Lee, T.G., Guo, X.L., Melito, S., Wang, K., Bayless, A.M., Wang, J.P., Hughes, T.J., Willis, D.K., Clemente, T.E., Diers, B.W., Jiang, J.M., Hudson, M.E. and Bent, A.F. (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science, 338, 1206-1209.
11. D'Auria, J.C., Chen, F. and Pichersky, E. (2002) Characterization of an acyltransferase capable of synthesizing benzylbenzoate and other volatile esters in flowers and damaged leaves of Clarkia breweri. Plant Physiol. 130, 466-476.
12. Doyle, E.A. and Lambert, K.N. (2003) Meloidogyne javanica chorismate mutase 1 alters plant cell development. Mol. Plant Microbe In. 16, 123-131.
13. Garcion, C., Lohmann, A., Lamodiere, E., Catinot, J., Buchala, A., Doermann, P. and Metraux, J.P. (2008) Characterization and biological function of the isochorismate synthase2 gene of Arabidopsis. Plant Physiol. 147, 1279-1287.
14. Ithal, N., Recknor, J., Nettleton, D., Hearne, L., Maier, T., Baum, T.J. and Mitchum, M.G. (2007) Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Mol. Plant Microbe In. 20, 293-305.
15. Kandoth, P.K., Ithal, N., Recknor, J., Maier, T., Nettleton, D., Baum, T.J. and Mitchum, M.G. (2011) The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates the expression of a large number of stress-and defense-related genes in degenerating feeding cells. Plant Physiol. 155, 1960-1975.
16. Kempster, V.N., Davies, K.A. and Scott, E.S. (2001) Chemical and biological induction of resistance to the clover cyst nematode (Heterodera trifolii) in white clover (Trifolium repens). Nematology, 3, 35-43.
17. Kereszt, A., Li, D., Indrasumunar, A., Nguyen, C.D.T., Nontachaiyapoom, S., Kinkema, M. and Gresshoff, P.M. (2007) Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat. Protocols. 2, 948-952.
18. Khan, R., Alkharouf, N., Beard, H., MacDonald, M., Chouikha, I., Meyer, S., Grefenstette, J., Knap, H. and Matthews, B. (2004) Microarray analysis of gene expression in soybean roots susceptible to the soybean cyst nematode two days post invasion. J. Nematol. 36, 241-248.
19. Klink, V.P., Overall, C.C., Alkharouf, N.W., MacDonald, M.H. and Matthews, B.F. (2007) A time-course comparative microarray analysis of an incompatible and compatible response by Glycine max (soybean) to Heterodera glycines (soybean cyst nematode) infection. Planta, 226, 1423-1447.
20. Klink, V.P., Kim, K.H., Martins, V., MacDonald, M., Beard, H., Alkharouf, N., Lee, S.K., Park, S.C. and Matthews, B.F. (2009) A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of development of female Heterodera glycines cyst formation during infection of Glycine max. Planta, 230, 53-71.
21. Klink, V.P., Overall, C.C., Alkharouf, N.W., MacDonald, M.H. and Matthews, B.F. (2010) Microarray detection call methodology as a means to identify and compare transcripts expressed within syncytial cells from soybean (Glycine max) roots undergoing resistant and susceptible reactions to the soybean cyst nematode (Heterodera glycines). J. Biomed Biotechnol. 2010, 491217.
22. Klink, V.P., Hosseini, P., Matsye, P.D., Alkharouf, N.W. and Matthews, B.F. (2011) Differences in gene expression amplitude overlie a conserved transcriptomic program occurring between the rapid and potent localized resistant reaction at the syncytium of the Glycine max genotype Peking (PI 548402) as compared to the prolonged and potent resistant reaction of PI 88788. Plant Mol. Biol. 75, 141-165.
23. Koenning, S.R. and Wrather, J.A. (2010) Suppression of soybean yield potential in the continental United States from plant diseases estimated from 2006 to 2009. Plant Health Prog. http://dx.doi.org/10.1094/PHP-2010-1122-01-RS.
24. Koo, Y., Kim, M., Kim, E., Song, J., Jung, C., Moon, J.K., Kim, J.H., Seo, H., Song, S., Kim, J.K., Lee, J., Cheong, J.J. and Choi, Y. (2007) Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol. Biol. 64, 1-15.
25. Liu, S.M., Kandoth, P.K., Warren, S.D., Yeckel, G., Heinz, R., Alden, J., Yang, C.L., Jamai, A., El-Mellouki, T., Juvale, P.S., Hill, J., Baum, T.J., Cianzio, S., Whitham, S.A., Korkin, D., Mitchum, M.G. and Meksem, K. (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature, 492, 256-260.
26. Lu, P., Shannon, J.G., Sleper, D.A., Nguyen, H.T., Cianzio, S.R. and Arelli, R. (2006) Genetics of cyst nematode resistance in soybean PIs 467312 and 507354. Euphytica, 149, 259-265.
27. Mann, D.G.J., Abercrombie, L.L., Rudis, M.R., Millwood, R.J., Dunlap, J.R. and Stewart, C.N. Jr. (2012) Very bright orange fluorescent plants: endoplasmic reticulum targeting of orange fluorescent proteins as visual reporters in transgenic plants. BMC Biotechnol. 12, 17.
28. Matson, A.L. and Williams, L.F. (1965) Evidence of a fourth gene for resistance to the soybean cyst nematode. Crop Sci. 5, 477.
29. Matsye, P.D., Kumar, R., Hosseini, P., Jones, C.M., Tremblay, A., Alkharouf, N.W., Matthews, B.F. and Klink, V.P. (2011) Mapping cell fate decisions that occur during soybean defense responses. Plant Mol. Biol. 77, 513-528.
30. Matthews, B.F., Beard, H., MacDonald, M.H., Kabir, S., Youssef, R.M., Hosseini, P. and Brewer, E. (2013) Engineered resistance and hypersusceptibility through functional metabolic studies of 100 genes in soybean to its major pathogen, the soybean cyst nematode. Planta, 237, 1337-1357.
31. Mazarei, M., Liu, W., Al-Ahmad, H., Arelli, P., Pantalone, V.R. and Stewart, C.N. Jr. (2011) Gene expression profiling of resistant and susceptible soybean lines infected with soybean cyst nematode. Theor. Appl. Genet. 123, 1193-1206.
32. Melito, S., Heuberger, A.L., Cook, D., Diers, B.W., MacGuidwin, A.E. and Bent, A.F. (2010) A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1 locus LRR-Kinase on soybean cyst nematode resistance. BMC Plant Biol. 10, 104.
33. Negre, F., Kolosova, N., Knoll, J., Kish, C.M. and Dudareva, N. (2002) Novel S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, an enzyme responsible for biosynthesis of methyl salicylate and methyl benzoate, is not involved in floral scent production in snapdragon flowers. Arch. Biochem. Biophys. 406, 261-270.
34. Park, S.W., Kaimoyo, E., Kumar, D., Mosher, S. and Klessig, D.F. (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science, 318, 113-116.
35. Pieterse, C.M.J. and Van Loon, L.C. (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr. Opin. Plant Biol. 7, 456-464.
36. Pott, M.B., Pichersky, E. and Piechulla, B. (2002) Evening specific oscillations of scent emission, SAMT enzyme activity, and SAMT mRNA in flowers of Stephanotis floribunda. J. Plant Physiol. 159, 925-934.
37. Pott, M.B., Hippauf, F., Saschenbrecker, S., Chen, F., Kiefer, I., Slusarenko, A., Ross, J., Noel, J.P., Pichersky, E., Effmert, U. and Piechulla, B. (2004) Biochemical and structural characterization of benzenoid carboxyl methyltransferases involved in floral scent production in Stephanotis floribunda and Nicotiana suaveolens. Plant Physiol. 135, 1946-1955.
38. Puthoff, D.P., Ehrenfried, M.L., Vinyard, B.T. and Tucker, M.L. (2007) GeneChip profiling of transcriptional responses to soybean cyst nematode, Heterodera glycines, colonization of soybean roots. J. Exp. Bot. 58, 3407-3418.
39. Qin, G., Gu, H., Zhao, Y., Ma, Z., Shi, G., Yang, Y., Pichersky, E., Chen, H., Liu, M., Chen, Z. and Qu, L. (2005) Regulation of auxin homeostasis and plant development by an indole-3-acetic acid carboxyl methyltransferase in Arabidopsis. Plant Cell, 17, 2693-2704.
40. Rao-Arelli, A.P., Anand, S.C. and Wrather, J.A. (1992) Soybean resistance to soybean cyst nematode race-3 is conditioned by an additional dominant gene. Crop Sci. 32, 862-864.
41. Rao-Arelli, A.P., Wilcox, J.A., Myers, O. and Gibson, P.T. (1997) Soybean germplasm resistant to races 1 and 2 of Heterodera glycines. Crop Sci. 37, 1367-1369.
42. Ross, J.R., Nam, K.H., D'Auria, J.C. and Pichersky, E. (1999) S-Adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch. Biochem. Biophys. 367, 9-16.
43. Sanchez-Rojo, S., Lopez-Delgado, H.A., Mora-Herrera, M.E., Almeyda-Leon, H.I., Zavaleta-Mancera, H.A. and Espinosa-Victoria, D. (2011) Salicylic acid protects potato plants-from phytoplasma-associated stress and improves tuber photosynthate assimilation. Am. J. Potato Res. 88, 175-183.
44. Sandhu, D., Tasma, I.M., Frasch, R. and Bhattacharyya, M.K. (2009) Systemic acquired resistance in soybean is regulated by two proteins, orthologous to Arabidopsis NPR1. BMC Plant Biol. 9, 105-119.
45. Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J.X., Mitros, T., Nelson, W., Hyten, D.L., Song, Q.J., Thelen, J.J., Cheng, J.L., Xu, D., Hellsten, U., May, G.D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, M.K., Sandhu, D., Valliyodan, B., Lindquist, E., Peto, M., Grant, D., Shu, S.Q., Goodstein, D., Barry, K., Futrell-Griggs, M., Abernathy, B., Du, J.C., Tian, Z.X., Zhu, L.C., Gill, N., Joshi, T., Libault, M., Sethuraman, A., Zhang, X.C., Shinozaki, K., Nguyen, H.T., Wing, R.A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D., Stacey, G., Shoemaker, R.C. and Jackson, S.A. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178-183.
46. Seo, H.S., Song, J.T., Cheong, J.J., Lee, Y.H., Lee, Y.W., Hwang, I., Lee, J.S. and Choi, Y.D. (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc. Natl Acad. Sci. USA, 98, 4788-4793.
47. Tieman, D., Zeigler, M., Schmelz, E., Taylor, M.G., Rushing, S., Jones, J.B. and Klee, H.J. (2010) Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J. 62, 113-123.
48. Varbanova, M., Yamaguchi, S., Yang, Y., McKelvey, K., Hanada, A., Borochov, R., Yu, F., Jikumaru, Y., Ross, J., Cortes, D., Ma, C.J., Noel, J.P., Mander, L., Shulaev, V., Kamiya, Y., Rodermel, S., Weiss, D. and Pichersky, E. (2007) Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell, 19, 32-45.
49. Wubben, M.J.E., Jin, J. and Baum, T.J. (2008) Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol. Plant Microbe In. 21, 424-432.
50. Yuan, J.S., Wang, D. and Stewart, C.N. Jr. (2008) Statistical methods for efficiency adjusted real-time PCR quantification. Biotechnol. J. 3, 112-123.
51. Zhao, N., Guan, J., Lin, H. and Chen, F. (2007) Molecular cloning and biochemical characterization of indole-3-acetic acid methyltransferase from poplar. Phytochemistry, 68, 1537-1544.
52. Zhao, N., Ferrer, J.L., Ross, J., Guan, J., Yang, Y., Pichersky, E., Noel, J.P. and Chen, F. (2008) Structural, biochemical, and phylogenetic analyses suggest that indole-3-acetic acid methyltransferase is an evolutionarily ancient member of the SABATH family. Plant Physiol. 146, 455-467.
53. Zhao, N., Guan, J., Ferrer, J.L., Engle, N., Chern, M., Ronald, P., Tschaplinski, T.J. and Chen, F. (2010) Biosynthesis and emission of insect-induced methyl salicylate and methyl benzoate from rice. Plant Physiol. Bioch. 48, 279-287.