Overexpression of a soybean 4-coumaric acid: coenzyme A ligase (GmPI4L) enhances resistance to Phytophthora sojae in soybean
Xi Chen A * , Xin Fang A * , Youyi Zhang A * , Xin Wang A B * , Chuanzhong Zhang A * , Xiaofei Yan A , Yuanling Zhao A C , Junjiang Wu D , Pengfei Xu A E and Shuzhen Zhang
A E
+ Author Affiliations
- Author Affiliations
A Soybean Research Institute, Key Laboratory of Soybean Biology of Chinese Education Ministry, Northeast Agricultural University, Harbin, Heilongjiang, China.
B Heilongjiang Academy of Land Reclamation Sciences, Harbin, Heilongjiang, China.
C Biotechnology Research Institute, Heilongjiang Academy of Agricultural Sciences, Harbin, China.
D Soybean Research Institute of Heilongjiang Academy of Agricultural Sciences, Key Laboratory of Soybean Cultivation of Ministry of Agriculture PR China, Harbin Heilongjiang, China.
E Corresponding authors. Email: xupengfei@neau.edu.cn; zhangshuzhen@neau.edu.cn
Functional Plant Biology 46(4) 304-313 https://doi.org/10.1071/FP18111
Submitted: 27 April 2018 Accepted: 18 October 2018 Published: 7 November 2018
Abstract
Phytophthora root and stem rot of soybean (Glycine max (L.) Merr.) caused by Phytophthora sojae is a destructive disease worldwide. The enzyme 4-coumarate: CoA ligase (4CL) has been extensively studied with regard to plant responses to pathogens. However, the molecular mechanism of the response of soybean 4CL to P. sojae remains unclear. In a previous study, a highly upregulated 4CL homologue was characterised through suppressive subtractive hybridisation library and cDNA microarrays, in the resistant soybean cultivar ‘Suinong 10’ after infection with P. sojae race 1. Here, we isolated the full-length EST, and designated as GmPI4L (P. sojae-inducible 4CL gene) in this study, which is a novel member of the soybean 4CL gene family. GmPI4L has 34–43% over all amino acid sequence identity with other plant 4CLs. Overexpression of GmPI4L enhances resistance to P. sojae in transgenic soybean plants. The GmPI4L is located in the cell membrane when transiently expressed in Arabidopsis protoplasts. Further analyses showed that the contents of daidzein, genistein, and the relative content of glyceollins are significantly increased in overexpression GmPI4L soybeans. Taken together, these results suggested that GmPI4L plays an important role in response to P. sojae infection, possibly by enhancing the content of glyceollins, daidzein, and genistein in soybean.
Additional keywords: GmPI4L, pathogenic change, Phytophthora sojae, soybean.
References
Agati G, Brunetti C, Ferdinando MD, Ferrini F, Pollastri S, Tattini M (2013) Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiology and Biochemistry 72, 35–45.| Functional roles of flavonoids in photoprotection: new evidence, lessons from the past.Crossref | GoogleScholarGoogle Scholar |
Bailey KL, Gossen BD, Gugel RK, Morrall RAA (2003) ‘Diseases of field crops in Canada.’ (Canadian Phytopathological Society: Saskatoon, SK, USA)
Baskar V, Venkatesh R, Ramalingam S (2018) Flavonoids (antioxidants systems) in higher plants and their response to stresses. In ‘Antioxidants and antioxidant enzymes in higher plants’. pp. 253–268. (Springer: Dordrecht, The Netherlands)
Becker-Andre M, Schulze-Lefert P, Hahlbrock K (1991) Structural comparison, modes of expression, and putative cis-acting elements of the two 4-coumarate: CoA ligase genes in potato. The Journal of Biological Chemistry 266, 8551–8559.
Bi C, Chen F, Jackson L, Gill BS, Li W (2011) Expression of lignin biosynthetic genes in wheat during development and upon infection by fungal pathogens. Plant Molecular Biology Reporter 29, 149–161.
| Expression of lignin biosynthetic genes in wheat during development and upon infection by fungal pathogens.Crossref | GoogleScholarGoogle Scholar |
Boué SM, Raina AK (2003) Effects of plant flavonoids on fecundity, survival, and feeding of the Formosan subterranean termite. Journal of Chemical Ecology 29, 2575–2584.
| Effects of plant flavonoids on fecundity, survival, and feeding of the Formosan subterranean termite.Crossref | GoogleScholarGoogle Scholar |
Boué SM, Carter CH, Ehrlich KC, Clevel TE (2000) Induction of the soybean phytoalexins coumestrol and glyceollin by Aspergillus. Journal of Agricultural and Food Chemistry 48, 2167–2172.
| Induction of the soybean phytoalexins coumestrol and glyceollin by Aspergillus.Crossref | GoogleScholarGoogle Scholar |
Boué SM, Tilghman SL, Elliott S, Zimmerman MC, Williams KY (2009) Identification of the potent phytoestrogen glycinol in elicited soybean (Glycine max). Endocrinology 150, 2446
| Identification of the potent phytoestrogen glycinol in elicited soybean (Glycine max).Crossref | GoogleScholarGoogle Scholar |
Chacón O, González M, López Y, Portieles R, Pujol M, González E, Schoonbeek HJ, Métraux JP, Borrás-Hidalgo O (2010) Over-expression of a protein kinase gene enhances the defense of tobacco against Rhizoctonia solani. Gene 452, 54–62.
| Over-expression of a protein kinase gene enhances the defense of tobacco against Rhizoctonia solani.Crossref | GoogleScholarGoogle Scholar |
Davies PJ (1995) The plant hormone concept: concentration, sensitivity and transport. In ‘Plant hormones physiology biochemistry and molecular biology’. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Dong LD, Cheng YX, Wu JJ, Cheng Q, Li WB, Fan SJ, Jiang LY, Xu ZL, Kong FJ, Zhang DY, Xu PF, Zhang SZ (2015) Overexpression of GmERF5, a new member of the soybean EAR motif-containing ERF transcription factor, enhances resistance to Phytophthora sojae in soybean. Journal of Experimental Botany 66, 2635–2647.
| Overexpression of GmERF5, a new member of the soybean EAR motif-containing ERF transcription factor, enhances resistance to Phytophthora sojae in soybean.Crossref | GoogleScholarGoogle Scholar |
Ehlting J, Büttner D, Wang Q, Douglas CJ, Somssich IE, Kombrink E (1999) Three 4-coumarate: coenzyme A ligases in Arabidopsis thaliana represent two evolutionary classes in angiosperms. The Plant Journal 19, 9–20.
| Three 4-coumarate: coenzyme A ligases in Arabidopsis thaliana represent two evolutionary classes in angiosperms.Crossref | GoogleScholarGoogle Scholar |
Eliceiri KW, Berthold MR, Goldberg IG (2012) Biological imaging software tools. Nature Methods 9, 697–710.
| Biological imaging software tools.Crossref | GoogleScholarGoogle Scholar |
Fehr WR, Caviness CE, Burmood DT, Pennington J (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Science 11, 929–931.
| Stage of development descriptions for soybeans, Glycine max (L.) Merrill.Crossref | GoogleScholarGoogle Scholar |
Gui J, Shen J, Li L (2011) Functional characterization of evolutionarily divergent 4-coumarate: coenzyme A ligases in rice. Plant Physiology 157, 574–586.
| Functional characterization of evolutionarily divergent 4-coumarate: coenzyme A ligases in rice.Crossref | GoogleScholarGoogle Scholar |
Guillaumie S, San-Clemente H, Deswarte C, Martinez Y, Lapierre C, Murigneux A, Barrière Y, Pichon M, Goffner D (2007) MAIZEWALL. Database and developmental gene expression profiling of cell wall biosynthesis and assembly in maize. Plant Physiology 143, 339–363.
| MAIZEWALL. Database and developmental gene expression profiling of cell wall biosynthesis and assembly in maize.Crossref | GoogleScholarGoogle Scholar |
Hahn MG, Bonhoff A, Grisebach H (1985) Quantitative localization of the phytoalexin glyceollin I in relation to fungal hyphae in soybean roots infected with Phytophthora megasperma f. sp. Glycinea. Plant Physiology 77, 591–601.
| Quantitative localization of the phytoalexin glyceollin I in relation to fungal hyphae in soybean roots infected with Phytophthora megasperma f. sp. Glycinea.Crossref | GoogleScholarGoogle Scholar |
Holsters M, Waele D, Depicker A, Messens E, Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Molecular & General Genetics 163, 181–187.
| Transfection and transformation of Agrobacterium tumefaciens.Crossref | GoogleScholarGoogle Scholar |
Jiao C, Yang R, Zhou Y, Gu Z (2016) Nitric oxide mediates isoflavone accumulation and the antioxidant system enhancement in soybean sprouts. Food Chemistry 204, 373–380.
| Nitric oxide mediates isoflavone accumulation and the antioxidant system enhancement in soybean sprouts.Crossref | GoogleScholarGoogle Scholar |
Kaufmann MJ, Gerdemann JW (1958) Root and stem rot of soybean caused by Phytophthora sojae n. sp. Phytopathology 48, 201–208.
Kim HJ, Suh HJ, Kim JH, Park S, Joo YC (2010) Antioxidant activity of glyceollins derived from soybean elicited with Aspergillus sojae. Journal of Medicinal Food 13, 382–390.
| Antioxidant activity of glyceollins derived from soybean elicited with Aspergillus sojae.Crossref | GoogleScholarGoogle Scholar |
Lee D, Ellard M, Wanner LA, Davis KR, Douglas CJ (1995) The Arabidopsis thaliana 4-coumarate: CoA ligase (4CL) gene stress and developmentally regulated expression and nucleotide sequence of its cDNA. Plant Molecular Biology 28, 871–884.
| The Arabidopsis thaliana 4-coumarate: CoA ligase (4CL) gene stress and developmentally regulated expression and nucleotide sequence of its cDNA.Crossref | GoogleScholarGoogle Scholar |
Li NH, Zhao M, Liu TF, Dong LD, Cheng Q, Wu JJ, Wang L, Chen X, Zhang CZ, Lu WC, Xu PF, Zhang SZ (2017) A novel soybean dirigent gene GmDIR22 contributes to promotion of lignan biosynthesis and enhances resistance to Phytophthora sojae. Frontiers of Plant Science 8, 1185
| A novel soybean dirigent gene GmDIR22 contributes to promotion of lignan biosynthesis and enhances resistance to Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar |
Lindermayr C, Möllers B, Fliegmann J, Uhlmann A, Lottspeich F, Meimberg H, Ebel J (2002) Divergent members of a soybean (Glycine max L.) 4-coumarate: coenzyme A ligase gene family. European Journal of Biochemistry 269, 1304–1315.
| Divergent members of a soybean (Glycine max L.) 4-coumarate: coenzyme A ligase gene family.Crossref | GoogleScholarGoogle Scholar |
Lois R, Hahlbrock K (1992) Differential wound activation of members of the phenylalanine ammonia-lyase and 4-coumarate: CoA ligase gene families in various organs of parsley plants. Zeitschrift Fur Naturforschung C 47, 90–94.
| Differential wound activation of members of the phenylalanine ammonia-lyase and 4-coumarate: CoA ligase gene families in various organs of parsley plants.Crossref | GoogleScholarGoogle Scholar |
Lygin AV, Hill CB, Zernova OV, Crull L, Widholm JM (2010) Response of soybean pathogens to glyceollin. Phytopathology 100, 897–903.
| Response of soybean pathogens to glyceollin.Crossref | GoogleScholarGoogle Scholar |
Lygin AV, Hill CB, Zernova OV, Crull L, Widholm JM (2013) Glyceollin is an important component of soybean plant defense against Phytophthora sojae and Macrophomina phaseolina. Phytopathology 103, 984–994.
| Glyceollin is an important component of soybean plant defense against Phytophthora sojae and Macrophomina phaseolina.Crossref | GoogleScholarGoogle Scholar |
Lyne RL, Mulheirn LJ, Leworthy DP (1976) New pterocarpinoid phytoalexins of soybean. Journal of the Chemical Society, Chemical Communications 13, 497–498.
| New pterocarpinoid phytoalexins of soybean.Crossref | GoogleScholarGoogle Scholar |
Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. The Plant Journal 29, 257–268.
| H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions.Crossref | GoogleScholarGoogle Scholar |
Mohr PG, Cahill DM (2001) Relative roles of glyceollin, lignin and the hypersensitive response and the influences of ABA in compatible and incompatible interactions of soybeans with Phytophthora sojae. Physiological and Molecular Plant Pathology 58, 31–41.
| Relative roles of glyceollin, lignin and the hypersensitive response and the influences of ABA in compatible and incompatible interactions of soybeans with Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar |
Morris PF, Savard ME, Ward EWB (1991) Identification and accumulation of isoflavonoids and isoflavone glucosides in soybean leaves and hypocotyls in resistance responses to Phytophthora megasperma f. sp. Glycinea. Physiological and Molecular Plant Pathology 39, 229–244.
| Identification and accumulation of isoflavonoids and isoflavone glucosides in soybean leaves and hypocotyls in resistance responses to Phytophthora megasperma f. sp. Glycinea.Crossref | GoogleScholarGoogle Scholar |
Morrison RH, Thorne JC (1978) Inoculation of detached cotyledons for screening soybeans against two races of Phytophthora megasperma var. sojae. Crop Science 18, 1089–1091.
| Inoculation of detached cotyledons for screening soybeans against two races of Phytophthora megasperma var. sojae.Crossref | GoogleScholarGoogle Scholar |
Nwachukwu ID, Luciano FB, Udenigwe CC (2013) The inducible soybean glyceollin phytoalexins with multifunctional health-promoting properties. Food Research International 54, 1208–1216.
| The inducible soybean glyceollin phytoalexins with multifunctional health-promoting properties.Crossref | GoogleScholarGoogle Scholar |
Pieterse CM, Leonreyes A, Van DES, Van Wees SC (2009) Networking by small molecule hormones in plant immunity. Nature Chemical Biology 5, 308–316.
| Networking by small molecule hormones in plant immunity.Crossref | GoogleScholarGoogle Scholar |
Ragg H, Kuhn DN, Hahlbrock K (1981) Coordinated regulation of 4-coumarate: CoA ligase and phenylalanine ammonia-lyase mRNAs in cultured plant cells. The Journal of Biological Chemistry 256, 10061–10065.
Rao GD, Pan X, Xu F, Zhang YZ, Cao S, Jiang XN (2015) Divergent and overlapping function of five 4-coumarate/coenzyme A ligases from Populus tomentosa. Plant Molecular Biology Reporter 33, 841–854.
| Divergent and overlapping function of five 4-coumarate/coenzyme A ligases from Populus tomentosa.Crossref | GoogleScholarGoogle Scholar |
Rastogi S, Kumar R, Chanotiya CS, Shanker K, Gupta MM, Nagegowda DA, Shasany AK (2013) 4-Coumarate: CoA ligase partitions metabolites for eugenol biosynthesis. Plant & Cell Physiology 54, 1238–1252.
| 4-Coumarate: CoA ligase partitions metabolites for eugenol biosynthesis.Crossref | GoogleScholarGoogle Scholar |
Saballos A, Sattler SE, Sanchez E, Foster TP, Xin Z, Kang C, Pedersen JF, Vermerris W (2012) Brown midrib2 (Bmr2) encodes the major 4-coumarate: coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench). The Plant Journal 70, 818–830.
| Brown midrib2 (Bmr2) encodes the major 4-coumarate: coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench).Crossref | GoogleScholarGoogle Scholar |
Schmelzer E, Kruger-Lebus S, Hahlbrock K (1989) Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves. The Plant Cell 1, 993–1001.
| Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves.Crossref | GoogleScholarGoogle Scholar |
Schmitthenner AF, Bhat RG (1994) Useful methods for studying Phytophthora in the laboratory. Ohio Agricultural Research and Development Center. Special circular 143.
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL (2010) Genome sequence of the palaeopolyploid soybean. Nature 463, 178–183.
| Genome sequence of the palaeopolyploid soybean.Crossref | GoogleScholarGoogle Scholar |
Sivankalyani V, Feygenberg O, Diskin S, Wright B, Alkan N (2016) Increased anthocyanin and flavonoids in mango fruit peel are associated with cold and pathogen resistance. Postharvest Biology and Technology 111, 132–139.
| Increased anthocyanin and flavonoids in mango fruit peel are associated with cold and pathogen resistance.Crossref | GoogleScholarGoogle Scholar |
Soltani BM, Ehlting J, Hamberger B, Douglas CJ (2006) Multiple cis-regulatory elements regulate distinct and complex patterns of developmental and wound-induced expression of Arabidopsis thaliana 4CL gene family members. Planta 224, 1226–1238.
| Multiple cis-regulatory elements regulate distinct and complex patterns of developmental and wound-induced expression of Arabidopsis thaliana 4CL gene family members.Crossref | GoogleScholarGoogle Scholar |
Sugano S, Sugimoto T, Takatsuji H, Jiang J (2013) Induction of resistance to Phytophthora sojae in soybean (Glycine max) by salicylic acid and ethylene. Plant Pathology 62, 1048–1056.
| Induction of resistance to Phytophthora sojae in soybean (Glycine max) by salicylic acid and ethylene.Crossref | GoogleScholarGoogle Scholar |
Sugimoto T, Kato M, Yoshida S, Matsumoto I, Kobayashi T (2012) Pathogenic diversity of Phytophthora sojae and breeding strategies to develop Phytophthora-resistant soybeans. Breeding Science 61, 511–522.
| Pathogenic diversity of Phytophthora sojae and breeding strategies to develop Phytophthora-resistant soybeans.Crossref | GoogleScholarGoogle Scholar |
Sun HY, Guo K, Feng SQ, Zou WH, Li Y, Fan CF, Peng LC (2015) Positive selection drives adaptive diversification of the 4-coumarate: CoA ligase (4CL) gene in angiosperms. Ecology and Evolution 5, 3413–3420.
| Positive selection drives adaptive diversification of the 4-coumarate: CoA ligase (4CL) gene in angiosperms.Crossref | GoogleScholarGoogle Scholar |
van Parijs FRD, Ruttink T, Boerjan W, Haesaert G, Byrne SL, Asp T, Roldán-Ruiz I, Muylle H (2015) Clade classification of monolignol biosynthesis gene family members reveals target genes to decrease lignin in Lolium perenne. Plant Biology 17, 877–892.
| Clade classification of monolignol biosynthesis gene family members reveals target genes to decrease lignin in Lolium perenne.Crossref | GoogleScholarGoogle Scholar |
Wang DD, Bai H, Chen WQ, Lu H, Jiang XN (2009) Identifying a cinnamoyl coenzyme A reductase (CCR) activity with 4-coumaric acid: coenzyme A ligase (4CL) reaction products in Populus tomentosa. Journal of Plant Biology 52, 482–491.
| Identifying a cinnamoyl coenzyme A reductase (CCR) activity with 4-coumaric acid: coenzyme A ligase (4CL) reaction products in Populus tomentosa.Crossref | GoogleScholarGoogle Scholar |
Ward EWB, Lazarovits G, Unwin CH, Buzzell RI (1979) Hypocotyl reactions and glyceollin in soybeans inoculated with zoospores of Phytophthora megaspuma var. sojae. Phytopathology 69, 951–955.
| Hypocotyl reactions and glyceollin in soybeans inoculated with zoospores of Phytophthora megaspuma var. sojae.Crossref | GoogleScholarGoogle Scholar |
Xu PF, Chen WY, Lv HY, Fan SJ, Wang X, Jiang LY (2012) Differentially expressed genes of soybean during infection by Phytophthora sojae. Journal of Integrative Agriculture 11, 368–377.
| Differentially expressed genes of soybean during infection by Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar |
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2, 1565–1572.
| Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis.Crossref | GoogleScholarGoogle Scholar |
Zeng GL, Li DM, Han YP, Teng WL, Wang J, Qiu LQ, Li WB (2009) Identification of QTL underlying isoflavone contents in soybean seeds among multiple environments. Theoretical and Applied Genetics 118, 1455–1463.
| Identification of QTL underlying isoflavone contents in soybean seeds among multiple environments.Crossref | GoogleScholarGoogle Scholar |
Zhang SZ, Xu PF, Wu JJ, Allen X, Zhang JX, Li WB, Chen C, Chen WY (2010) Races of Phytophthora sojae and their virulences on commonly grown soybean varieties in Heilongjiang, China. Plant Disease 94, 87–91.
| Races of Phytophthora sojae and their virulences on commonly grown soybean varieties in Heilongjiang, China.Crossref | GoogleScholarGoogle Scholar |
Zhang EH, Guo XF, Meng ZF, Wang J, Sun J, Yao X, Xun H (2015) Construction, expression, and characterization of Arabidopsis thaliana 4CL and Arachis hypogaea RS fusion gene 4CL:RS in Escherichia coli. World Journal of Microbiology & Biotechnology 31, 1379–1385.
| Construction, expression, and characterization of Arabidopsis thaliana 4CL and Arachis hypogaea RS fusion gene 4CL:RS in Escherichia coli.Crossref | GoogleScholarGoogle Scholar |
Zhang CZ, Wang X, Zhang F, Dong LD, Wu JJ, Cheng Q, Qi DY, Yan XF, Jiang LY, Fan SJ, Li NH, Li DM, Xu PF, Zhang SZ (2017) Phenylalanine ammonia-lyase2.1 contributes to the soybean response towards Phytophthora sojae infection. Scientific Reports 7, 7242
| Phenylalanine ammonia-lyase2.1 contributes to the soybean response towards Phytophthora sojae infection.Crossref | GoogleScholarGoogle Scholar |
