Research Progress in Benzoxazinoids in Plants

doi:10.13560/j.cnki.biotech.bull.1985.2024-0497

Abstract

Abstract:

Plant secondary metabolites are important components of regulators and defense substances that regulate growth and development, and their compound types are extremely complex. Benzoxazinoids (BXs), as one of the secondary metabolites of the alkaloid family, have natural plant active ingredients and are used in the fields of pharmaceutical ingredients and food additives. Their pharmacological and health effects have become a new research hotspot. At present, the study on BXs compounds is concentrated on gramineae corn and wheat, and the research on their regulatory mechanisms is not in-depth enough. In this paper, the secondary metabolic process of BXs compounds is introduced in detail from the composition, classification and metabolic pathways. The evolutionary characteristics indicate that they have a unique biosynthetic cluster structure. It is summarized that BXs compounds play a defensive role in plant growth and development, including defense against insects, microbial interactions and allelopathy in competing plants. Moreover, BXs serve as signaling molecules that mediate plant chelation of metal ions, respond to external environmental stimuli and participate in the regulators of plant hormones, revealing the important function of BXs compounds in the interaction between plants and environmental conditions. Concurrently, it summarizes the issues and solutions faced by BXs compounds in the current research. It is believed that with the in-depth research of BXs compounds, it will surely promote the development of new agricultural production and sustainable strategic practices, help to deeply explore their potential application value, and solve the multiple challenges facing current agricultural and forestry production.

Key words: benzoxazinoids, secondary metabolism, biosynthesis, defense, allelopathy, signaling molecule

LI Xiao-ming, SHANG Xiu-hua, WANG You-shuang, WU Zhi-hua. Research Progress in Benzoxazinoids in Plants[J]. Biotechnology Bulletin, 2025, 41(4): 9-20.

Figures/Tables 7

References 109

1	Hartmann T. From waste products to ecochemicals: fifty years research of plant secondary metabolism [J]. Phytochemistry, 2007, 68(22/23/24): 2831-2846.
2	Fernie AR, Pichersky E. Focus issue on metabolism: metabolites, metabolites everywhere [J]. Plant Physiol, 2015, 169(3): 1421-1423.
3	Erb M, Kliebenstein DJ. Plant secondary metabolites as defenses, regulators, and primary metabolites: the blurred functional trichotomy [J]. Plant Physiol, 2020, 184(1): 39-52.
4	Li YQ, Kong DX, Fu Y, et al. The effect of developmental and environmental factors on secondary metabolites in medicinal plants [J]. Plant Physiol Biochem, 2020, 148: 80-89.
5	Adhikari KB, Tanwir F, Gregersen PL, et al. Benzoxazinoids: Cereal phytochemicals with putative therapeutic and health-protecting properties [J]. Mol Nutr Food Res, 2015, 59(7): 1324-1338.
6	Yang L, Wen KS, Ruan X, et al. Response of plant secondary metabolites to environmental factors [J]. Molecules, 2018, 23(4): 762.
7	Bennett RN, Wallsgrove RM. Secondary metabolites in plant defence mechanisms [J]. New Phytol, 1994, 127(4): 617-633.
8	Patra B, Schluttenhofer C, Wu YM, et al. Transcriptional regulation of secondary metabolite biosynthesis in plants [J]. Biochim Biophys Acta, 2013, 1829(11): 1236-1247.
9	Ma ZQ, Li SS, Zhang MJ, et al. Light intensity affects growth, photosynthetic capability, and total flavonoid accumulation of Anoectochilus plants [J]. HortScience, 2010, 45(6): 863-867.
10	Sanchita, Sharma A. Gene expression analysis in medicinal plants under abiotic stress conditions [M]//Plant Metabolites and Regulation Under Environmental Stress. Amsterdam: Elsevier, 2018: 407-414.
11	Wink M. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective [J]. Phytochemistry, 2003, 64(1): 3-19.
12	朱三明, 郑敏敏, 田恬, 等. 植物次生代谢途径与调控研究进展 [J]. 植物生理学报, 2023, 59(12): 2188-2216.
	Zhu SM, Zheng MM, Tian T, et al. Research progress on plant secondary metabolism and regulation [J]. Plant Physiol J, 2023, 59(12): 2188-2216.
13	朱璐, 袁冲, 刘义飞. 植物次生代谢产物生物合成基因簇研究进展 [J]. 植物学报, 2024, 59(1): 134-143.
	Zhu L, Yuan C, Liu YF. Research progress on plant secondary metabolite biosynthetic gene clusters [J]. Chin Bull Bot, 2024, 59(1): 134-143.
14	Dixon RA, Strack D. Phytochemistry meets genome analysis, and beyond [J]. Phytochemistry, 2003, 62(6): 815-816.
15	de Bruijn WJC, Vincken JP, Duran K, et al. Mass spectrometric characterization of benzoxazinoid glycosides from Rhizopus-elicited wheat (Triticum aestivum) seedlings [J]. J Agric Food Chem, 2016, 64(32): 6267-6276.
16	Hanhineva K, Rogachev I, Aura AM, et al. Qualitative characterization of benzoxazinoid derivatives in whole grain rye and wheat by LC-MS metabolite profiling [J]. J Agric Food Chem, 2011, 59(3): 921-927.
17	Niemeyer HM. Hydroxamic acids derived from 2-hydroxy-2H-1, 4-benzoxazin-3(4H)-one: key defense chemicals of cereals [J]. J Agric Food Chem, 2009, 57(5): 1677-1696.
18	Sicker D, Frey M, Schulz M, et al. Role of natural benzoxazinones in the survival strategy of plants [J]. Int Rev Cytol, 2000, 198: 319-346.
19	Frey M, Chomet P, Glawischnig E, et al. Analysis of a chemical plant defense mechanism in grasses [J]. Science, 1997, 277(5326): 696-699.
20	Von Rad U, Hüttl R, Lottspeich F, et al. Two glucosyltransferases are involved in detoxification of benzoxazinoids in maize [J]. Plant J, 2001, 28(6): 633-642.
21	Jonczyk R, Schmidt H, Osterrieder A, et al. Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7 [J]. Plant Physiol, 2008, 146(3): 1053-1063.
22	Sue M, Nakamura C, Nomura T. Dispersed benzoxazinone gene cluster: molecular characterization and chromosomal localization of glucosyltransferase and glucosidase genes in wheat and rye [J]. Plant Physiol, 2011, 157(3): 985-997.
23	Bakera B, Makowska B, Groszyk J, et al. Structural characteristics of ScBx genes controlling the biosynthesis of hydroxamic acids in rye (Secale cereale L.) [J]. J Appl Genet, 2015, 56(3): 287-298.
24	Kriechbaumer V, Weigang LD, Fiesselmann A, et al. Characterisation of the tryptophan synthase alpha subunit in maize [J]. BMC Plant Biol, 2008, 8: 44.
25	Spiteller P, Glawischnig E, Gierl A, et al. Studies on the biosynthesis of 2-hydroxy-1, 4-benzoxazin-3-one (HBOA) from 3-hydroxyindolin-2-one in Zea mays [J]. Phytochemistry, 2001, 57(3): 373-376.
26	Meihls LN, Handrick V, Glauser G, et al. Natural variation in maize aphid resistance is associated with 2, 4-dihydroxy-7-methoxy-1, 4-benzoxazin-3-one glucoside methyltransferase activity [J]. Plant Cell, 2013, 25(6): 2341-2355.
27	Handrick V, Robert CAM, Ahern KR, et al. Biosynthesis of 8-O-methylated benzoxazinoid defense compounds in maize [J]. Plant Cell, 2016, 28(7): 1682-1700.
28	Frey M, Schullehner K, Dick R, et al. Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants [J]. Phytochemistry, 2009, 70(15/16): 1645-1651.
29	Niculaes C, Abramov A, Hannemann L, et al. Plant protection by benzoxazinoids—recent insights into biosynthesis and function [J]. Agronomy, 2018, 8(8): 143.
30	Nützmann HW, Huang AC, Osbourn A. Plant metabolic clusters from genetics to genomics [J]. New Phytol, 2016, 211(3): 771-789.
31	Wisecaver JH, Borowsky AT, Tzin V, et al. A global coexpression network approach for connecting genes to specialized metabolic pathways in plants [J]. Plant Cell, 2017, 29(5): 944-959.
32	Zheng LL, McMullen MD, Bauer E, et al. Prolonged expression of the BX1 signature enzyme is associated with a recombination hotspot in the benzoxazinoid gene cluster in Zea mays [J]. J Exp Bot, 2015, 66(13): 3917-3930.
33	Dutartre L, Hilliou F, Feyereisen R. Phylogenomics of the benzoxazinoid biosynthetic pathway of Poaceae: gene duplications and origin of the Bx cluster [J]. BMC Evol Biol, 2012, 12: 64.
34	Nomura T, Nasuda S, Kawaura K, et al. Structures of the three homoeologous loci of wheat benzoxazinone biosynthetic genes TaBx3 and TaBx4 and characterization of their promoter sequences [J]. Theor Appl Genet, 2008, 116(3): 373-381.
35	Rokas A, Wisecaver JH, Lind AL. The birth, evolution and death of metabolic gene clusters in fungi [J]. Nat Rev Microbiol, 2018, 16(12): 731-744.
36	Wittkopp PJ, Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence [J]. Nat Rev Genet, 2011, 13(1): 59-69.
37	Nomura T, Ishihara A, Yanagita RC, et al. Three genomes differentially contribute to the biosynthesis of benzoxazinones in hexaploid wheat [J]. Proc Natl Acad Sci U S A, 2005, 102(45): 16490-16495.
38	Tzin V, Fernandez-Pozo N, Richter A, et al. Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays [J]. Plant Physiol, 2015, 169(3): 1727-1743.
39	Song J, Liu H, Zhuang HF, et al. Transcriptomics and alternative splicing analyses reveal large differences between maize lines B73 and Mo17 in response to aphid Rhopalosiphum padi infestation [J]. Front Plant Sci, 2017, 8: 1738.
40	Yan F, Liang X, Zhu X. The role of DIMBOA on the feeding of Asian corn borer, Ostrinia furnacalis (Guenée) (Lep., Pyralidae) [J]. J Appl Entomol, 1999, 123(1): 49-53.
41	Yan FM, Xu CR, Li SG, et al. Effects of DIMBOA on several enzymatic systems in Asian corn borer, Ostrinia furnacalis (Guenée) [J]. J Chem Ecol, 1995, 21(12): 2047-2056.
42	Hedin PA, Davis FM, Williams WP. 2-hydroxy-4, 7-dimethoxy-1,4-benzoxazin-3-one (N-O-Me-DIMBOA), a possible toxic factor in corn to the southwestern corn borer [J]. J Chem Ecol, 1993, 19(3): 531-542.
43	Campos F, Donskov N, Arnason TJ, et al. Biological effects and toxicokinetics of DIM BOA in Diadegma terebrans (Hymenoptera: Ichneumonidae), an endoparasitoid of Ostrinia nubilalis (Lepidoptera: Pyralidae) [J]. J Econ Entomol, 1990, 83(2): 356-360.
44	Tzin V, Hojo Y, Strickler SR, et al. Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding [J]. J Exp Bot, 2017, 68(16): 4709-4723.
45	Yang X, Hafeez M, Chen HY, et al. DIMBOA-induced gene expression, activity profiles of detoxification enzymes, multi-resistance mechanisms, and increased resistance to indoxacarb in tobacco cutworm, Spodoptera litura (Fabricius) [J]. Ecotoxicol Environ Saf, 2023, 267: 115669.
46	Robert CA, Zhang X, Machado RA, et al. Sequestration and activation of plant toxins protect the western corn rootworm from enemies at multiple trophic levels [J]. eLife, 2017, 6: e29307.
47	Sikder MM, Vestergård M, Kyndt T, et al. Benzoxazinoids selectively affect maize root-associated nematode taxa [J]. J Exp Bot, 2021, 72(10): 3835-3845.
48	Israni B, Wouters FC, Luck K, et al. The fall armyworm Spodoptera frugiperda utilizes specific UDP-glycosyltransferases to inactivate maize defensive benzoxazinoids [J]. Front Physiol, 2020, 11: 604754.
49	Israni B, Luck K, Römhild SCW, et al. Alternative transcript splicing regulates UDP-glucosyltransferase-catalyzed detoxification of DIMBOA in the fall armyworm (Spodoptera frugiperda) [J]. Sci Rep, 2022, 12(1): 10343.
50	Xie YS, Arnason JT, Philogène BJR, et al. Role of 2, 4-dihydroxy-7-methoxy-1, 4-benzoxazin-3-one (DIMBOA) in the resistance of maize to western corn rootworm, Diabrotica virgifera virgifera (Leconte) (Coleoptera: Chrysomelidae) [J]. Can Entomol, 1990, 122(6): 1177-1186.
51	Malook SU, Qi JF, Hettenhausen C, et al. The oriental armyworm (Mythimna separata) feeding induces systemic defence responses within and between maize leaves [J]. Philos Trans R Soc Lond B Biol Sci, 2019, 374(1767): 20180307.
52	Klun JA, Tipton CL, Brindley TA. 2, 4-dihydroxy-7-methoxy-1, 4-benzoxazin-3-one (DIMBOA), an active agent in the resistance of maize to the European corn borer [J]. J Econ Entomol, 1967, 60(6): 1529-1533.
53	Maag D, Köhler A, Robert CAM, et al. Highly localized and persistent induction of Bx1-dependent herbivore resistance factors in maize [J]. Plant J, 2016, 88(6): 976-991.
54	Givovich A, Morse S, Cerda H, et al. Hydroxamic acid glucosides in honeydew of aphids feeding on wheat [J]. J Chem Ecol, 1992, 18(6): 841-846.
55	Zhang ZF, Lan H, Cao HH, et al. Impacts of constitutive and induced benzoxazinoids levels on wheat resistance to the grain aphid (Sitobion avenae) [J]. Metabolites, 2021, 11(11): 783.
56	Batyrshina ZS, Shavit R, Yaakov B, et al. The transcription factor TaMYB31 regulates the benzoxazinoid biosynthetic pathway in wheat [J]. J Exp Bot, 2022, 73(16): 5634-5649.
57	Etzerodt T, Gislum R, Laursen BB, et al. Correlation of deoxynivalenol accumulation in Fusarium-infected winter and spring wheat cultivars with secondary metabolites at different growth stages [J]. J Agric Food Chem, 2016, 64(22): 4545-4555.
58	Etzerodt T, Maeda K, Nakajima Y, et al. 2, 4-dihydroxy-7-methoxy-2H-1, 4-benzoxazin-3(4H)-one (DIMBOA) inhibits trichothecene production by Fusarium graminearum through suppression of Tri6 expression [J]. Int J Food Microbiol, 2015, 214: 123-128.
59	Ridenour JB, Bluhm BH. The novel fungal-specific gene FUG1 has a role in pathogenicity and fumonisin biosynthesis in Fusarium verticillioides [J]. Mol Plant Pathol, 2017, 18(4): 513-528.
60	Ding XP, Yang M, Huang HC, et al. Priming maize resistance by its neighbors: activating 1, 4-benzoxazine-3-ones synthesis and defense gene expression to alleviate leaf disease [J]. Front Plant Sci, 2015, 6: 830.
61	Zhang XS, Huang TZ, Wang QC, et al. Mechanisms of resistance to spot blotch in Yunnan iron shell wheat based on metabolome and transcriptomics [J]. Int J Mol Sci, 2022, 23(9): 5184.
62	Song YY, Cao M, Xie LJ, et al. Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight [J]. Mycorrhiza, 2011, 21(8): 721-731.
63	Święcicka M, Dmochowska-Boguta M, Orczyk W, et al. Changes in benzoxazinoid contents and the expression of the associated genes in rye (Secale cereale L.) due to brown rust and the inoculation procedure [J]. PLoS One, 2020, 15(5): e0233807.
64	Cen ZX, Hu BJ, Yang SY, et al. Mechanism of benzoxazinoids affecting the growth and development of Fusarium oxysporum f. sp. fabae [J]. Plant Mol Biol, 2024, 114(3): 42.
65	Ma GL, Hu BJ, Yang SY, et al. Benzoxazinoids secreted by wheat root weaken the pathogenicity of Fusarium oxysporum f.sp. fabae by inhibiting linoleic acid and nucleotide metabolisms [J]. Plant Cell Rep, 2024, 43(4): 109.
66	Huffaker A, Dafoe NJ, Schmelz EA. ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance [J]. Plant Physiol, 2011, 155(3): 1325-1338.
67	Venturelli S, Belz RG, Kämper A, et al. Plants release precursors of histone deacetylase inhibitors to suppress growth of competitors [J]. Plant Cell, 2015, 27(11): 3175-3189.
68	Oikawa A, Ishihara A, Tanaka C, et al. Accumulation of HDMBOA-Glc is induced by biotic stresses prior to the release of MBOA in maize leaves [J]. Phytochemistry, 2004, 65(22): 2995-3001.
69	Li YH, Xia ZC, Kong CH. Allelobiosis in the interference of allelopathic wheat with weeds [J]. Pest Manag Sci, 2016, 72(11): 2146-2153.
70	Liu HX, An T, Zhao YF, et al. Benzoxazines in the root exudates responsible for nonhost disease resistance of maize to Phytophthora sojae [J]. Phytopathology, 2022, 112(7): 1537-1544.
71	Kong CH, Wang P, Gu Y, et al. Fate and impact on microorganisms of rice allelochemicals in paddy soil [J]. J Agric Food Chem, 2008, 56(13): 5043-5049.
72	Li XJ, Xia ZC, Kong CH, et al. Mobility and microbial activity of allelochemicals in soil [J]. J Agric Food Chem, 2013, 61(21): 5072-5079.
73	Hazrati H, Fomsgaard IS, Kudsk P. Root-exuded benzoxazinoids: uptake and translocation in neighboring plants [J]. J Agric Food Chem, 2020, 68(39): 10609-10617.
74	Zhang CL, Li XW, Chen YQ, et al. Effects of Eucalyptus litter and roots on the establishment of native tree species in Eucalyptus plantations in South China [J]. For Ecol Manag, 2016, 375: 76-83.
75	Williams RA. Mitigating biodiversity concerns in Eucalyptus plantations located in South China [J]. J Biosci Med, 2015, 3(6): 1-8.
76	Jabeen R, Yamada K, Shigemori H, et al. Induction of ß-glucosidase activity in maize coleoptiles by blue light illumination [J]. J Plant Physiol, 2006, 163(5): 538-545.
77	Epstein WW, Rowsemitt CN, Berger PJ, et al. Dynamics of 6-methoxybenzoxazolinone in winter wheat: effects of photoperiod and temperature [J]. J Chem Ecol, 1986, 12(10): 2011-2020.
78	Bakera B, Święcicka M, Stochmal A, et al. Benzoxazinoids biosynthesis in rye (Secale cereale L.) is affected by low temperature [J]. Agronomy, 2020, 10(9): 1260.
79	Wang XF, Chen QY, Wu YY, et al. Genome-wide analysis of transcriptional variability in a large maize-teosinte population [J]. Mol Plant, 2018, 11(3): 443-459.
80	Erb M, Köllner TG, Degenhardt J, et al. The role of abscisic acid and water stress in root herbivore-induced leaf resistance [J]. New Phytol, 2011, 189(1): 308-320.
81	Sutour S, Doan VC, Mateo P, et al. Isolation and structure determination of drought-induced multihexose benzoxazinoids from maize (Zea mays) [J]. J Agric Food Chem, 2024, 72(7): 3427-3435.
82	Zhang F, Wu JF, Sade N, et al. Genomic basis underlying the metabolome-mediated drought adaptation of maize [J]. Genome Biol, 2021, 22(1): 260.
83	Erb M, Gordon-Weeks R, Flors V, et al. Belowground ABA boosts aboveground production of DIMBOA and primes induction of chlorogenic acid in maize [J]. Plant Signal Behav, 2009, 4(7): 636-638.
84	冯远娇, 金琼, 王建武. 机械损伤对Bt玉米化学防御的系统诱导效应 [J]. 植物生态学报, 2010, 34(6): 695-703.
	Feng YJ, Jin Q, Wang JW. Systemic induced effects of mechanical wounding on the chemical defense of Bt corn (Zea mays) [J]. Chin J Plant Ecol, 2010, 34(6): 695-703.
85	Vaughan MM, Huffaker A, Schmelz EA, et al. Interactive effects of elevated [CO₂] and drought on the maize phytochemical defense response against mycotoxigenic Fusarium verticillioides [J]. PLoS One, 2016, 11(7): e0159270.
86	Robert CAM, Mateo P. The chemical ecology of benzoxazinoids [J]. Chimia, 2022, 76(11): 928-938.
87	Bi HH, Luang S, Li Y, et al. Identification and characterization of wheat drought-responsive MYB transcription factors involved in the regulation of cuticle biosynthesis [J]. J Exp Bot, 2016, 67(18): 5363-5380.
88	Guyer A, van Doan C, Maurer C, et al. Climate change modulates multitrophic interactions between maize, a root herbivore, and its enemies [J]. J Chem Ecol, 2021, 47(10/11): 889-906.
89	Petho M. Possible role of cyclic hydroxamic acids in the iron uptake by grasses[J]. Acta Agronomica Hungarica, 1993, 42: 203-214.
90	Aciksoz SB, Ozturk L, Gokmen OO, et al. Effect of nitrogen on root release of phytosiderophores and root uptake of Fe(III)-phytosiderophore in Fe-deficient wheat plants [J]. Physiol Plant, 2011, 142(3): 287-296.
91	Hu LF, Wu ZW, Robert CAM, et al. Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth [J]. Proc Natl Acad Sci U S A, 2021, 118(43): e2109602118.
92	Poschenrieder C, Tolrà RP, Barceló J. A role for cyclic hydroxamates in aluminium resistance in maize? [J]. J Inorg Biochem, 2005, 99(9): 1830-1836.
93	Clark RT, Famoso AN, Zhao KY, et al. High-throughput two-dimensional root system phenotyping platform facilitates genetic analysis of root growth and development [J]. Plant Cell Environ, 2013, 36(2): 454-466.
94	Guimaraes CT, Simoes CC, Pastina MM, et al. Genetic dissection of Al tolerance QTLs in the maize genome by high density SNP scan [J]. BMC Genomics, 2014, 15(1): 153.
95	Zhao ZK, Gao XF, Ke Y, et al. A unique aluminum resistance mechanism conferred by aluminum and salicylic-acid-activated root efflux of benzoxazinoids in maize [J]. Plant Soil, 2019, 437(1): 273-289.
96	Ye JR, Zhong T, Zhang DF, et al. The auxin-regulated protein ZmAuxRP1 coordinates the balance between root growth and stalk rot disease resistance in maize [J]. Mol Plant, 2019, 12(3): 360-373.
97	Venis MA, Watson PJ. Naturally occuring modifiers of auxin-receptor interaction in corn: identification as benzoxazolinones [J]. Planta, 1978, 142(1): 103-107.
98	Feng YJ, Wang XY, Du TT, et al. Effects of salicylic acid concentration and post-treatment time on the direct and systemic chemical defense responses in maize (Zea mays L.) following exogenous foliar application [J]. Molecules, 2022, 27(20): 6917.
99	Feng YJ, Wang XY, Du TT, et al. Effects of exogenous salicylic acid application to aboveground part on the defense responses in Bt (Bacillus thuringiensis) and Non-Bt corn (Zea mays L.) seedlings [J]. Plants (Basel), 2022, 11(16): 2162.
100	冯远娇, 王建武, 骆世明. 外源茉莉酸处理对Bt玉米直接防御物质含量及其相关基因表达的影响 [J]. 中国农业科学, 2007, 40(11): 2481-2487.
	Feng YJ, Wang JW, Luo SM. Effects of exogenous jasmonic acid on concentrations of direct defense chemicals and expression of related genes in Bt (Bacillus thuringiensis) corn (Zea mays) [J]. Sci Agric Sin, 2007, 40(11): 2481-2487.
101	Oikawa A, Ishihara A, Iwamura H. Induction of HDMBOA-Glc accumulation and DIMBOA-Glc 4-O-methyltransferase by jasmonic acid in poaceous plants [J]. Phytochemistry, 2002, 61(3): 331-337.
102	Frébortová J, Novák O, Frébort I, et al. Degradation of cytokinins by maize cytokinin dehydrogenase is mediated by free radicals generated by enzymatic oxidation of natural benzoxazinones [J]. Plant J, 2010, 61(3): 467-481.
103	Zhang CP, Li J, Li S, et al. ZmMPK6 and ethylene signalling negatively regulate the accumulation of anti-insect metabolites DIMBOA and DIMBOA-Glc in maize inbred line A188 [J]. New Phytol, 2021, 229(4): 2273-2287.
104	赵媛. 小麦幼苗中丁布的含量、异株克生活性与诱导效应研究 [D]. 杨凌: 西北农林科技大学, 2005.
	Zhao Y. Study on the content, allogram activity and induction effect of Butachlor in wheat seedlings [D]. Yangling: Northwest A & F University, 2005.
105	郑永权. 小麦幼苗中丁布的含量、活性与诱导效应研究 [D]. 武汉: 华中师范大学, 2004.
	Zheng YQ. Study on the content, activity and induction effect of butachlor in wheat seedlings [D]. Wuhan: Central China Normal University, 2004.
106	Kato-Noguchi H. Effects of four benzoxazinoids on gibberellin-induced alpha-amylase activity in barley seeds [J]. J Plant Physiol, 2008, 165(18): 1889-1894.
107	Nakajima E, Hasegawa K, Yamada K, et al. Effects of the auxin-inhibiting substances raphanusanin and benzoxazolinone on apical dominance of pea seedlings [J]. Plant Growth Regul, 2001, 35(1): 11-15.
108	Sue M, Fujii M, Fujimaki T. Increased benzoxazinoid (Bx) levels in wheat seedlings via jasmonic acid treatment and etiolation and their effects on Bx genes including Bx6 [J]. Biochem Biophys Rep, 2021, 27: 101059.
109	Oikawa A, Ishihara A, Hasegawa M, et al. Induced accumulation of 2-hydroxy-4, 7-dimethoxy-1, 4-benzoxazin-3-one glucoside (HDMBOA-Glc) in maize leaves [J]. Phytochemistry, 2001, 56(7): 669-675.

分类 Classification		缩写 Abbreviation	化学全称 Chemical name
分类 Classification		缩写 Abbreviation	化学全称 Chemical name	R1		R2	R3
苯并噁嗪酮	异羟肟酸	DIBOA	2，4-二羟基-1，4苯并噁嗪-3-酮	H	H		H
Benzoxaziones		DIMBOA	2，4-二羟基-7-甲氧基-1，4苯并噁嗪-4-酮	H	OCH₃		H
		TRIBOA	2，4，7-三羟基-1，4苯并噁嗪-3-酮	H	OH		H
		TRIMBOA	2，4，7-三羟基-8-甲氧基-1，4苯并噁嗪-3-酮	H	OH		OCH₃
		DIM₂BOA	2，4-二羟基-7，8-二甲氧基-1，4苯并噁嗪-3-酮	H	OCH₃		OCH₃
	内酰胺	HBOA	2-羟基-2H-1，4-苯并噁嗪-3（4H）-酮	H	H		H
		DHBOA	2，7-二羟基-1，4-苯并噁嗪-3-酮	H	OH		H
		HMBOA	2-羟基-7-甲氧基-2H-1，4-苯并噁嗪-3（4H）-酮	H	OCH₃		H
		HM₂BOA	2-羟基-6，7-二甲氧基-2H-1，4-苯并噁嗪-3（4H）-酮	H	OCH₃		OCH₃
	甲基肟酸	HDMBOA	2-羟基-4，7-二甲氧基-1，4-苯并噁嗪-3-酮	H	OCH₃		H
	甲基肟酸	HDM₂BOA	2-羟基-4，7，8-三甲氧基-1，4-苯并噁嗪-3-酮	H	OCH₃		OCH₃
苯并噁嗪唑啉酮 Benzoxazolinones		BOA	2-苯并噁唑啉-2（3H）酮	H	H		H
		MBOA	6-甲氧基-苯并噁唑啉-2-酮	H	OCH₃		H
		M₂BOA	2-羟基-2H-1，4-苯并噁嗪-3（4）酮	H	OCH₃		OCH₃

分类 Classification		缩写 Abbreviation	化学全称 Chemical name
分类 Classification		缩写 Abbreviation	化学全称 Chemical name	R1		R2	R3
苯并噁嗪酮	异羟肟酸	DIBOA	2，4-二羟基-1，4苯并噁嗪-3-酮	H	H		H
Benzoxaziones		DIMBOA	2，4-二羟基-7-甲氧基-1，4苯并噁嗪-4-酮	H	OCH₃		H
		TRIBOA	2，4，7-三羟基-1，4苯并噁嗪-3-酮	H	OH		H
		TRIMBOA	2，4，7-三羟基-8-甲氧基-1，4苯并噁嗪-3-酮	H	OH		OCH₃
		DIM₂BOA	2，4-二羟基-7，8-二甲氧基-1，4苯并噁嗪-3-酮	H	OCH₃		OCH₃
	内酰胺	HBOA	2-羟基-2H-1，4-苯并噁嗪-3（4H）-酮	H	H		H
		DHBOA	2，7-二羟基-1，4-苯并噁嗪-3-酮	H	OH		H
		HMBOA	2-羟基-7-甲氧基-2H-1，4-苯并噁嗪-3（4H）-酮	H	OCH₃		H
		HM₂BOA	2-羟基-6，7-二甲氧基-2H-1，4-苯并噁嗪-3（4H）-酮	H	OCH₃		OCH₃
	甲基肟酸	HDMBOA	2-羟基-4，7-二甲氧基-1，4-苯并噁嗪-3-酮	H	OCH₃		H
	甲基肟酸	HDM₂BOA	2-羟基-4，7，8-三甲氧基-1，4-苯并噁嗪-3-酮	H	OCH₃		OCH₃
苯并噁嗪唑啉酮 Benzoxazolinones		BOA	2-苯并噁唑啉-2（3H）酮	H	H		H
		MBOA	6-甲氧基-苯并噁唑啉-2-酮	H	OCH₃		H
		M₂BOA	2-羟基-2H-1，4-苯并噁嗪-3（4）酮	H	OCH₃		OCH₃

基因 Gene	定位 Location	编码酶 Encoding enzyme	生化功能 Biochemical function
BX1	叶绿体	吲哚-3-甘油磷酸裂解酶	Indole-3-glycerophosphate→Indole
BX2	内质网	细胞色素P450单加氧酶CYP71C4	Indole→DIBOA
BX3	内质网	细胞色素P450单加氧酶CYP71C2
BX4	内质网	细胞色素P450单加氧酶CYP71C1
BX5	内质网	细胞色素P450单加氧酶CYP71C3
BX6	细胞质	2-酮戊二酸依赖型双加氧酶	GDIBOA→GTRIBOA
BX7	细胞质	O-甲基转移酶	GTRI（M）BOA→GDIMBOA/GDIM₂BOA
BX8	液泡	UDP-葡萄糖基转移酶	DIBOA→GDIBOA
BX9	液泡	UDP-葡萄糖基转移酶	DIBOA→GDIBOA
BX10	细胞质	O-甲基转移酶	GDIMBOA→GHDMBOA
BX11	细胞质	O-甲基转移酶
BX12	细胞质	O-甲基转移酶
BX13	细胞质	2-酮戊二酸依赖型双加氧酶	GDIMBOA→GTRIMBOA
BX14	细胞质	O-甲基转移酶	GDIM₂BOA→GHDM₂BOA

基因 Gene	定位 Location	编码酶 Encoding enzyme	生化功能 Biochemical function
BX1	叶绿体	吲哚-3-甘油磷酸裂解酶	Indole-3-glycerophosphate→Indole
BX2	内质网	细胞色素P450单加氧酶CYP71C4	Indole→DIBOA
BX3	内质网	细胞色素P450单加氧酶CYP71C2
BX4	内质网	细胞色素P450单加氧酶CYP71C1
BX5	内质网	细胞色素P450单加氧酶CYP71C3
BX6	细胞质	2-酮戊二酸依赖型双加氧酶	GDIBOA→GTRIBOA
BX7	细胞质	O-甲基转移酶	GTRI（M）BOA→GDIMBOA/GDIM₂BOA
BX8	液泡	UDP-葡萄糖基转移酶	DIBOA→GDIBOA
BX9	液泡	UDP-葡萄糖基转移酶	DIBOA→GDIBOA
BX10	细胞质	O-甲基转移酶	GDIMBOA→GHDMBOA
BX11	细胞质	O-甲基转移酶
BX12	细胞质	O-甲基转移酶
BX13	细胞质	2-酮戊二酸依赖型双加氧酶	GDIMBOA→GTRIMBOA
BX14	细胞质	O-甲基转移酶	GDIM₂BOA→GHDM₂BOA

序号 Serial No.	昆虫 Insect	功能描述 Functional description	参考 Reference
1	蚜虫	利用蚜虫侵染玉米自交系后转录和代谢水平均发生显著变化，其中ZmBX1、ZmBX2和ZmBX6基因的突变增加了蚜虫的繁殖	［38］［39］
2	玉米螟虫	玉米中4个转录因子ZmWRKY75、ZmMYB61、ZmNAC35和ZmGRAS37的表达与ZmBX1的表达模式相关，可能解释蚜虫侵染后苯并噁嗪类水平的变化；叶片摄食抗性与羟肟酸浓度呈正相关，DIMBOA具有与羟肟酸浓度相当的摄食威慑作用，影响幼虫神经系统酶和解毒酶的活性；西南玉米螟的抗性与HDMBOA的存在相关，对饲料中的幼虫具有毒性作用； DIMBOA和MBOA均增加了幼虫的死亡率和化蛹的发育时间，且与浓度水平呈正相关	［40-41］［42］［43］
3	甜菜夜蛾	甜菜夜蛾侵染玉米后基因表达和代谢图谱在1 h内发生迅速改变，ZmBX1和ZmBX2的突变显著改善了幼虫的生长	［44］
4	斜纹夜蛾	经过DIMBOA预处理的幼虫对各类杀虫剂产生高抗性，转录组分析发现解毒酶对斜纹夜蛾基因表达发挥重要作用	［45］
5	玉米根虫	玉米根中施加DIMBOA会增加玉米根虫的死亡率，根系BXs含量与抗毒性呈显著正相关	［46］
6	玉米线虫	玉米根中BXs化合物的浓度与线虫序列读数的相对丰度呈负相关，但与线虫类群之间存在正相关	［47］
7	草地贪夜蛾	草地贪夜蛾通过UDP-葡萄糖基转移酶进行立体选择性重新葡萄糖基化，对DIMBOA进行解毒； UGT33和UGT40参与苯并噁嗪的糖基化，并参与对草地贪夜蛾幼虫的解毒；模拟草地贪夜蛾取食后BXs含量增加，启动子和共表达分析表明，转录因子ZmbHLH57与ZmWRKY34调控系统叶片中的BXs生物合成基因	［48］［49］［50］
8	小麦球茎蝇	MBOA对幼虫的吸引呈剂量依赖性，并可能促进分泌物活性，而DIMBOA引起的反应较弱，因为土壤中MBOA比DIMBOA更稳定	［51］