Abstract
Crop varieties exhibited phenotype variations during domestication and breeding. Such phenotype variations include secondary metabolism differentiation; however, the underlying mechanisms remain to be clarified. Here, two elite maize inbred lines Mo17 and HZ4 were analyzed to determine constitutive phytoalexin accumulation including zealexins and kauralexins. Both inbred lines produced phytoalexins in above- and belowground tissues in sterile culture. HZ4 accumulated much more kauralexin A3 than Mo17, which was consistent with higher gene expression of kauralexin biosynthesis in HZ4. Promoter cloning and sequence analysis disclosed a number of sequence variations including fragment insertion/deletion and nucleotide substitution in promoter regions of both inbred lines. Further analysis showed that one key biosynthetic gene (KSL5) of maize phytoalexins exhibited higher promoter activity in HZ4 than in Mo17. The underlying mechanism was explored and promoter mutation in both inbred lines accounted for such promoter activity difference. Specifically, one W-box element with a positive effect in KSL5 promoter from HZ4 was identified; meanwhile, a 413-bp fragment in KSL5 promoter from Mo17 played a negative role in gene expression. Both inbred lines accumulated these sequence mutations in promoters during breeding, which resulted in different gene expression and phytoalexin production, potentially contributing to basic resistance.
Similar content being viewed by others
References
Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681
Agerbirk N, Olsen CE (2012) Glucosinolate structures in evolution. Phytochemistry 77:16–45
Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends Plant Sci 17:73–90
Christensen SA, Sims J, Vaughan M, Hunter C, Block A, Willett D, Alborn HT, Huffaker A, Schmelz EA. 2018. Commercial hybrids and mutant genotypes reveal complex protective roles for inducible terpenoid defenses. LID - https://doi.org/10.1093/jxb/erx495 [doi]. J Exp Bot
Ding Y, Huffaker A, Köllner TG, Weckwerth P, Robert CAM, Spencer JL, Lipka AE, Schmelz EA (2017) Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance. Plant Physiol 175:1455–1468
Ding Y, Murphy KM, Poretsky E, Mafu S, Yang B, Char SN, Christensen SA, Saldivar E, Wu M, Wang Q, Ji L, Schmitz RJ, Kremling KA, Buckler ES, Shen Z, Briggs SP, Bohlmann J, Sher A, Castro-Falcon G, Hughes CC, Huffaker A, Zerbe P, Schmelz EA (2019) Multiple genes recruited from hormone pathways partition maize diterpenoid defences. Nature Plants 5:1043–1056
Duan D, Fischer S, Merz P, Bogs J, Riemann M, Nick P (2016) An ancestral allele of grapevine transcription factor MYB14 promotes plant defence. J Exp Bot 67:1795–1804
Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696–699
Fu J, Liu Q, Wang C, Liang J, Liu L, Wang Q (2018) ZmWRKY79 positively regulates maize phytoalexin biosynthetic gene expression and is involved in stress response. J Exp Bot 69:497–510
Fu J, Ren F, Lu X, Mao H, Xu M, Degenhardt J, Peters RJ, Wang Q (2016) A tandem array of ent-kaurene synthases in maize with roles in gibberellin and more specialized metabolism. Plant Physiol 170:742–751
Harris LJ, Saparno A, Johnston A, Prisic S, Xu M, Allard S, Kathiresan A, Ouellet T, Peters RJ (2005) The maize An2 gene is induced by Fusarium attack and encodes an ent-copalyl diphosphate synthase. Plant Mol Biol 59:881–894
Hasegawa M, Mitsuhara I, Seo S, Okada K, Yamane H, Iwai T, Ohashi Y (2014) Analysis on blast fungus-responsive characters of a flavonoid phytoalexin sakuranetin; accumulation in infected rice leaves, antifungal activity and detoxification by fungus. Molecules 19:11404–11418
Huffaker A, Kaplan F, Vaughan MM, Dafoe NJ, Ni X, Rocca JR, Alborn HT, Teal PE, Schmelz EA (2011) Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize. Plant Physiol 156:2082–2097
Jeandet P, Courote E, Clement C, Ricord S, Crouzet J, Aziz A, Cordelier S (2017) Molecular engineering of phytoalexins in plants: benefits and limitations for food and agriculture. J Agric Food Chem 65:2643–2644
Jeandet P, Hebrard C, Deville M-A, Cordelier S, Dorey S, Aziz A, Crouzet J (2014) Deciphering the role of phytoalexins in plant-microorganism interactions and human health. Molecules 19:18033–18056
Kollner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008a) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20:482–494
Kollner TG, Schnee C, Li S, Svatos A, Schneider B, Gershenzon J, Degenhardt J (2008b) Protonation of a neutral (S)-beta-bisabolene intermediate is involved in (S)-beta-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. J Biol Chem 283:20779–20788
Kroymann J (2011) Natural diversity and adaptation in plant secondary metabolism. Curr Opin Plant Biol 14:246–251
Liang J, Liu J, Brown R, Jia M, Zhou K, Peters RJ, Wang Q (2018) Direct production of dihydroxylated sesquiterpenoids by a maize terpene synthase. Plant J 94:847–856
Liu L, White MJ, MacRae TH (1999) Transcription factors and their genes in higher plants functional domains, evolution and regulation. Eur J Biochem 262:247–257
Mafu S, Ding Y, Murphy KM, Yaacoobi O, Addison JB, Wang Q, Shen Z, Briggs SP, Bohlmann J, Castro-Falcon G, Hughes CC, Betsiashvili M, Huffaker A, Schmelz EA, Zerbe P (2018) Discovery, biosynthesis, and stress-related accumulation of dolabradiene-derived defenses in maize. Plant Physiol 176:2677–2690
Mao H, Liu J, Ren F, Peters RJ, Wang Q (2016) Characterization of CYP71Z18 indicates a role in maize zealexin biosynthesis. Phytochemistry 121:4–10
Mikkelsen MD, Petersen BL, Olsen CE, Halkier BA (2002) Biosynthesis and metabolic engineering of glucosinolates. Amino Acids 22:279–295
Mitsuhara I, Ugaki M, Hirochika H, Ohshima M, Murakami T, Gotoh Y, Katayose Y, Nakamura S, Honkura R, Nishimiya S, Ueno K, Mochizuki A, Tanimoto H, Tsugawa H, Otsuki Y, Ohashi Y (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol 37:49–59
Neilson EH, Goodger JQ, Woodrow IE, Moller BL (2013) Plant chemical defense: at what cost? Trends Plant Sci 18:250–258
Oikawa A, Ishihara A, Hasegawa M, Kodama O, Iwamura H (2001) Induced accumulation of 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside (HDMBOA-Glc) in maize leaves. Phytochemistry 56:669–675
Park S, Ahn IS, Kim JH, Lee MR, Kim JS, Kim HJ (2010) Glyceollins, one of the phytoalexins derived from soybeans under fungal stress, enhance insulin sensitivity and exert insulinotropic actions. J Agric Food Chem 58:1551–1557
Pedras MS, Yaya EE, Glawischnig E (2011) The phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat Prod Rep 28:1381–1405
Schmelz EA, Huffaker A, Sims JW, Christensen SA, Lu X, Okada K, Peters RJ (2014) Biosynthesis, elicitation, and roles of monocot terpenoid phytoalexins. Plant J 79:659–678
Schmelz EA, Kaplan F, Huffaker A, Dafoe NJ, Vaughan MM, Ni X, Rocca JR, Alborn HT, Teal PE (2011) Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc Natl Acad Sci U S A 108:5455–5460
Tamogami S, Rakwal R, Kodama O (1997) Phytoalexin production by amino acid conjugates of jasmonic acid through induction of naringenin-7-O-methyltransferase, a key enzyme on phytoalexin biosynthesis in rice (Oryza sativa L.). FEBS Lett 401:239–242
Xu M, Galhano R, Wiemann P, Bueno E, Tiernan M, Wu W, Chung IM, Gershenzon J, Tudzynski B, Sesma A, Peters RJ (2012) Genetic evidence for natural product-mediated plant-plant allelopathy in rice (Oryza sativa). New Phytol 193:570–575
Zimmermann MC, Tilghman SL, Boue SM, Salvo VA, Elliott S, Williams KY, Skripnikova EV, Ashe H, Payton-Stewart F, Vanhoy-Rhodes L, Fonseca JP, Corbitt C, Collins-Burow BM, Howell MH, Lacey M, Shih BY, Carter-Wientjes C, Cleveland TE, McLachlan JA, Wiese TE, Beckman BS, Burow ME (2010) Glyceollin I, a novel antiestrogenic phytoalexin isolated from activated soy. J Pharmacol Exp Ther 332:35–45
Funding
This work was supported by the funds of NSFC (31671708 and 31971825) to QW.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key message
Two maize inbred lines were identified to accumulate phytoalexins constitutively with different abundance, correlated to different biosynthetic gene expression of phytoalexins. These gene expression differences were characterized to be determined by promoter mutations that played positive or negative roles to regulate gene expression and might be accumulated during breeding.
Rights and permissions
About this article
Cite this article
Yang, P., Fu, J., Liang, J. et al. Promoter Variation Results in Differential Phytoalexin Accumulation in Two Maize Inbred Lines. Plant Mol Biol Rep 38, 165–174 (2020). https://doi.org/10.1007/s11105-019-01190-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-019-01190-1