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Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (9): 1295-1302.doi: 10.3724/SP.J.1006.2019.93003

• REVIEW •     Next Articles

Mechanisms underlying plant resistance to the acetohydroxyacid synthase- inhibiting herbicides

XU Qian-Yu1,LAN Yu2,LIU Jia-Xin2,ZHOU Xin-Yu3,ZHANG Gang3,ZHENG Zhi-Fu1,*()   

  1. 1 School of Agriculture and Food Science, Zhejiang A&F University, Hangzhou 311300, Zhejiang, China;
    2 School of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, Zhejiang, China;
    3 Wendeng Jiahe Seed Corporation, Ltd., Weihai 264400, Shandong, China
  • Received:2019-01-02 Accepted:2019-05-22 Online:2019-09-12 Published:2019-06-05
  • Contact: Zhi-Fu ZHENG E-mail:zzheng@zafu.edu.cn
  • Supported by:
    This study was supported by the National Natural Science Foundation of China(31871660)

Abstract:

The acetohydroxyacid synthase (AHAS)-inhibiting herbicides have been widely used in agricultural industry. However, the herbicides can sometimes cause phytotoxicity for those crops susceptible to them. Thus, it is important to create a series of new crop varieties resistant to different types of herbicides. This review presents our current understanding about the categories and characteristics of the AHAS-inhibiting herbicides, the properties of their respective target enzymes and their roles in the synthesis of branched chain amino acids, and the mechanisms underlying two types of plant resistance to the herbicides (namely, target- and non-target-site-based resistance), as well as our perspectives on the future trends in these research areas, which is expected to promote the research and development of herbicide-resistant crops.

Key words: acetohydroxyacid synthase, herbicide, target-site-based resistance, non-target-site-based resistance

[1] Godfray H C J, Beddington J R, Crute I R, Haddad L, Lawrence D, Muir J F, Pretty J, Robinson S, Thomas S M, Toulmin C . Food security: the challenge of feeding 9 billion people. Science, 2010,327:812-818.
[2] Tester M, Langridge P . Breeding technologies to increase crop production in a changing world. Science, 2010,327:818-822.
[3] Davis A S, Hill J D, Chase C A, Johanns A M, Liebman M . Increasing cropping system diversity balances productivity, profitability and environmental health. PLoS One, 2012,7:e47149, doi: 10.1371/journal.pone.0047149.
[4] Gianessi L P, Reigner N P . The value of herbicides in U.S. crop production. Weed Tech, 2007,21:559-566.
[5] Ding X X, Li P W, Zhou H Y, Li J, Bai Y Z . Comparative study on maximum residue limits standards of pesticides in peanuts. Chin J Oil Crop Sci, 2011,33:527-531 (in Chinese with English abstract).
[6] Jabusch T W, Tjeerdema R S . Chemistry and fate of triazolopyrimidine sulfonamide herbicides. Rev Environ Contamin Toxicol, 2008,193:31-52.
[7] Cui H L, Li X, Wang G, Wang J, Wei S, Cao H . Acetolactate synthase proline (197) mutations confer tribenuron-methyl resistance in Capsella bursa-pastoris populations from China. Pest Biochem Physiol, 2012,102:229-232.
[8] Han X J, Dong Y, Sun X N, Li X F, Zheng M Q . Molecular basis of resistance to tribenuron-methyl in Descurainia sophia(L.) populations from China. Pest Biochem Physiol, 2012,104:77-81.
[9] Lee H, Ullrich S E, Burke I C, Yenish J, Paulitz T C . Interactions between the root pathogen Rhizoctonia solani AG-8 and acetolactate-synthase-inhibiting herbicides in barley. Pest Manag Sci, 2012,68:845-852.
[10] Liu W, Bi Y, Li L, Yuan G, Wang J . Molecular basis of resistance to tribenuron in water starwort (Myosoton aquaticum) populations from China. Weed Sci, 2013,61:390-395.
[11] Yu H, Zhang F, Wang G, Liu Y, Liu D . Partial deficiency of isoleucine impairs root development and alters transcript levels of the genes involved in branched-chain amino acid and glucosinolate metabolism in Arabidopsis. J Exp Bot, 2013,64:599-612.
[12] Ouellet T, Rutledge R G, Miki B L . Members of the acetohydroxyacid synthase multigene family of Brassica napus has divergent patterns of expression. Plant J, 1992,2:321-330.
[13] Breccia G, Vega T, Felitti S A, Picardi L, Nestares G . Differential expression of acetohydroxyacid synthase genes in sunflower plantlets and its response to imazapyr herbicide. Plant Sci, 2013,208:28-33.
[14] Ochogavía A C, Breccia G, Vega T, Felitti S A, Picardi L A, Nestares G . Acetohydroxyacid synthase activity and transcripts profiling reveal tissue-specific regulation of ahas genes in sunflower. Plant Sci, 2014,224:144-150.
[15] Binder S . Branched-chain amino acid metabolism in Arabidopsis thaliana. Arabidopsis Book, 2010,8:e0137, doi: 10.1199/tab. 0137.
[16] Pratelli R, Pilot G . Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot, 2014,65:5535-5556.
[17] Shaner D L, Anderson P C, Stidham M A . Imidazolinones: potent inhibitors of acetohydroxyacid synthase. Plant Physiol, 1984,76:545-546.
[18] Duggleby R G, McCourt J A, Guddat L W . Structure and mechanism of inhibition of plant acetohydroxyacid synthase. Plant Physiol Biochem, 2008,46:309-324.
[19] Subramanian M V, Gerwick B C . Inhibition of acetolactate synthase by triazolopyrimidines. A review of recent developments. ACS Symp Ser Am Chem Soc, 1989,398:277-288.
[20] Subramanian M V, Hung H Y, Dias J M, Miner V M, Butler J H, Jachetta J J . Properties of mutant acetolactate synthases resistant to triazolopyrimidine sulfonanilide. Plant Physiol, 1990,94:239-244.
[21] Singh B K, Shaner D L . Biosynthesis of branched chain amino acids: From test tube to field. Plant Cell, 1995,7:935-944.
[22] Lee H, Rustgi S, Kumar N, Burke I, Yenish J P, Gill K S, von Wettstein D, Ullrich S E . Single nucleotide mutation in the barley acetohydroxy acid synthase (AHAS) gene confers resistance to imidazolinone herbicides. Proc Natl Acad Sci USA, 2011,108:8909-8913.
[23] Hershey H P, Schwartz L J, Gale J P, Abell L M . Cloning and functional expression of the small subunit of acetolactate synthase from Nicotiana plumbaginifolia. Plant Mol Biol, 1999,40:795-806.
[24] Lee Y T, Duggleby R G . Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry, 2001,40:6836-6844.
[25] Chen H, Saksa K, Zhao F, Qiu J, Xiong L . Genetic analysis of pathway regulation for enhancing branched-chain amino acid biosynthesis in plants. Plant J, 2010,63:573-583.
[26] Endo M, Shimizu T, Fujimori T, Yanagisawa S, Toki S . Herbicide-resistant mutations in acetolactate synthase can reduce feedback inhibition and lead to accumulation of branched-chain amino acids. Food Nutr Sci, 2013,4:522-528.
[27] Holmberg S, Petersen J G . Regulation of isoleucine-valine biosynthesis in Saccharomyces cerevisiae. Curr Genet, 1988,13:207-217.
[28] Gao J Q, Pu H M, Qi C K, Zhang J F, Long W H, Hu M L, Chen S, Chen X J, Chen F, Gu H . Identification of imidazolidone-resistant oilseed rape mutant. J Plant Genet Resour, 2010,11:369-373 (in Chinese with English abstract).
[29] Rajasekaran K, Grula J W, Anderson D M . Selection and characterization of mutant cotton (Gossypium hirsutum L.) cell lines resistant to sulfonylurea and imidazolinone herbicides. Plant Sci, 1996,199:115-124.
[30] Wright T R, Penner D . Cell selection and inheritance of imidazolinone resistance in sugar beet (Beta vulgaris). Theor Appl Genet, 1998,96:612-620.
[31] Kolkman J M, Slabaugh M B, Bruniard J M, Berry S, Bushman B S, Olungu C, Maes N, Abratti G, Zambelli A, Miller J F, Leon A, Knapp S J . Acetohydroxyacid synthase mutations conferring resistance to imidazolinone or sulfonylurea herbicides in sunflower. Theor Appl Genet, 2004,109:1147-1159.
[32] Pozniak C J, Birk I T, O’Donoughue L S, Ménard C, Hucl P J, Singh B K . Physiological and molecular characterization of mutation-derived imidazolinone resistance in spring wheat. Crop Sci, 2004,44:1434-1443.
[33] Tan S, Evans R R, Dahmer M L, Singh B K, Shaner D L . Imidazolinone-tolerant crops: History, current status and future. Pest Manag Sci, 2005,61:246-257.
[34] Sala C A, Bulos M, Echarte M, Whitt S R, Ascenzi R . Molecular and biochemical characterization of an induced mutation conferring imidazolinone resistance in sunflower. Theor Appl Genet, 2008,118:105-112.
[35] Sala C A, Bulos M . Inheritance and molecular characterization of broad range tolerance to herbicides targeting acetohydroxyacid synthase in sunflower. Theor Appl Genet, 2012,124:355-364.
[36] Powles S B, Yu Q . Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol, 2010,61:317-347.
[37] Ghio C, Ramos M L, Altieri E, Bulos M, Sala C A . Molecular characterization of Als1, an acetohydroxyacid synthase mutation conferring resistance to sulfonylurea herbicides in soybean. Theor Appl Genet, 2013,126:2957-2968.
[38] Walter K L, Strachan S D, Ferry N M, Albert H H, Castle L A, Sebastian S A . Molecular and phenotypic characterization of Als1 and Als2 mutations conferring tolerance to acetolactate synthase herbicides in soybean. Pest Manag Sci, 2014,70:1831-1839.
[39] Tranel P J, Wright T R . Resistance of weeds to ALS-inhibiting herbicides: What have we learned? Weed Sci, 2002,50:700-712.
[40] Bernasconi P, Woodworth A R, Rosen B A, Subramanian M V, Siehl D L . A naturally occurring point mutation confers broad range tolerance to herbicides that target acetolactate synthase. J Biol Chem, 1995,270:17381-17385.
[41] Jander G, Baerson S R, Hudak J A, Gonzalez K A, Gruys K J, Last R L . Ethylmethanesulfonate saturation mutagenesis in Arabidopsis to determine frequency of herbicide resistance. Plant Physiol, 2003,131:139-146.
[42] Haughn G W, Smith J, Mazur B, Somerville C . Transformation with a mutant Arabidopsis acetolactate synthase allele renders tobacco resistant to sulfonylureas. Mol Gen Genet, 1988,211:266-271.
[43] Lee K Y, Townsend J, Tepperman J, Black M, Chui C F, Mazur B, Dunsmuir P, Bedbrook J . The molecular basis of sulfonylurea herbicide resistance in tobacco. EMBO J, 1988,7:1241-1248.
[44] Liu W, Yuan G, Du L, Guo W, Li L, Bi Y, Wang J . A novel Pro197Glu substitution in acetolactate synthase (ALS) confers broad-spectrum resistance across ALS inhibitors. Pestic Biochem Physiol, 2015,117:31-38.
[45] Ntoanidou S, Kaloumenos N, Diamantidis G, Madesis P, Eleftherohorinos I . Molecular basis of Cyperus difformis cross- resistance to ALS-inhibiting herbicides. Pestic Biochem Physiol, 2016,127:38-45.
[46] Deng W, Yang Q, Zhang Y, Jiao H, Mei Y, Li X, Zheng M . Cross-resistance patterns to acetolactate synthase (ALS)-inhibiting herbicides of flixweed (Descurainia sophia L.) conferred by different combinations of ALS isozymes with a Pro-197-Thr mutation or a novel Trp-574-Leu mutation. Pestic Biochem Physiol, 2017,136:41-45.
[47] Rey-Caballero J, Menéndez J, Osuna M D, Salas M, Torra J . Target-site and non-target-site resistance mechanisms to ALS inhibiting herbicides in Papaver rhoeas. Pestic Biochem Physiol, 2017,138:57-65.
[48] Hattori J, Brown D, Mourad G, Labbé H, Ouellet T, Sunohara G, Rutledge R, King J, Miki B . An acetohydroxy acid synthase mutant reveals a single site involved in multiple herbicide resistance. Mol Gen Genet, 1995,246:419-425.
[49] Li J, Li M, Gao X, Fang F . A novel amino acid substitution Trp574Arg in acetolactate synthase (ALS) confers broad resistance to ALS-inhibiting herbicides in crabgrass (Digitaria sanguinalis). Pest Manag Sci, 2017,73:2538-2543.
[50] Pang S S, Guddat L W, Duggleby R G . Molecular basis of sulfonylurea herbicide inhibition of acetohydroxyacid synthase. J Biol Chem, 2003,278:7639-7644.
[51] Petit C, Duhieu B, Boucansaud K, Délye C . Complex genetic control of non-target-site-based resistance to herbicides inhibiting acetyl-coenzyme A carboxylase and acetolactate-synthase in Alopecurus. Plant Sci, 2010,178:501-509.
[52] Scarabel L, Pernin F, Délye C . Occurrence, genetic control and evolution of non-target-site based resistance to herbicides inhibiting acetolactate synthase (ALS) in the dicot weed Papaver rhoeas. Plant Sci, 2015,238:158-169.
[53] Yang Q, Deng W, Li X, Yu Q, Bai L, Zheng M . Target-site and non-target-site based resistance to the herbicide tribenuron- methyl in flixweed (Descurainia sophia L.). BMC Genomics, 2016,17:551-563 .
[54] Mei Y, Si C, Liu M, Qiu L, Zheng M . Investigation of resistance levels and mechanisms to nicosulfuron conferred by non-target- site mechanisms in large crabgrass (Digitaria sanguinalis L.) from China. Pestic Biochem Physiol, 2017,141:84-89.
[55] Zhao B, Fu D, Yu Y, Huang C, Yan K, Li P, Shafi J, Zhu H, Wei S, Ji M . Non-target-site resistance to ALS-inhibiting herbicides in a Sagittaria trifolia L. population. Pestic Biochem Physiol, 2017,140:79-84.
[56] Chen G, Xu H, Zhang T, Bai C, Dong L . Fenoxaprop-P-ethyl resistance conferred by cytochrome P450s and target site mutation in Alopecurus japonicus. Pest Manag Sci, 2018. doi: 10.1002/ps.4863.
[57] Tehranchian P, Nandula V, Jugulam M, Putta K, Jasieniuk M . Multiple resistance to glyphosate, paraquat and ACCase-inhibiting herbicides in Italian ryegrass populations from California: confirmation and mechanisms of resistance. Pest Manage Sci, 2017, doi: 10.1002/ps.4774.
[58] Oliveira M C, Gaines T A, Dayan F E, Patterson E L, Jhala A J, Knezevic S Z . Reversing resistance to tembotrione in an Amaranthus tuberculatus(var. rudis) population from Nebraska, USA with cytochrome P450 inhibitors. Pest Manag Sci, 2017, doi: 10.1002/ps.4697.
[59] Siminszky B, Corbin F T, Ward E R, Fleischmann T J, Dewey R E . Expression of a soybean cytochrome P450 monooxygenase cDNA in yeast and tobacco enhances the metabolism of phenylurea herbicides. Proc Natl Acad Sci USA, 1999,96:1750-1755.
[60] Saika H, Horita J, Taguchi-Shiobara F, Nonaka S, Nishizawa-Yokoi A, Iwakami S, Hori K, Matsumoto T, Tanaka T, Itoh T, Yano M, Kaku K, Shimizu T, Toki S . A novel rice cytochrome P450 gene, CYP72A31, confers tolerance to acetolactate synthase-inhibiting herbicides in rice and Arabidopsis. Plant Physiol, 2014,166:1232-1240.
[61] Yu Q, Powles S B . Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci, 2014,70:1340-1350.
[62] Pan L, Gao H, Xia W, Zhang T, Dong L . Establishing a herbicide-metabolizing enzyme library in Beckmannia syzigachne to identify genes associated with metabolic resistance. J Exp Bot, 2016,67:1745-1757.
[63] Burns E E, Keith B K, Refai M Y, Bothner B, Dyer W E . Proteomic and biochemical assays of glutathione-related proteins in susceptible and multiple herbicide resistant Avena fatua L. Pestic Biochem Physiol, 2017,140:69-78.
[64] Burns E E, Keith B K, Refai M Y, Bothner B, Dyer W E . Constitutive redox and phosphoproteome changes in multiple herbicide resistant Avena fatua L. are similar to those of systemic acquired resistance and systemic acquired acclimation. J Plant Physiol, 2018,220:105-114.
[65] Li Z, Liu Z B, Xing A, Moon B P, Koellhoffer J P, Huang L, Ward R T, Clifton E, Falco S C, Cigan A M . Cas9-guide RNA directed genome editing in soybean. Plant Physiol, 2015,169:960-970.
[66] Svitashev S, Young J K, Schwartz C, Gao H, Falco S C, Cigan A M . Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using Cas9 and guide RNA. Plant Physiol, 2015,169:931-945.
[67] Komor A C, Kim Y B, Packer M S, Zuris J A, Liu D R . Programmable editing of a target base in genomic DNA without double stranded DNA cleavage. Nature, 2016,533:420-424.
[68] Chen Y, Wang Z, Ni H, Xu Y, Chen Q, Jiang L . CRISPR/Cas9- mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. Sci China Life Sci, 2017,60:520-523.
[69] Shimatani Z, Kashojiya S, Takayama M, Terada R, Arazoe T, Ishii H, Teramura H, Yamamoto T, Komatsu H, Miura K . Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol, 2017,35:441-443.
[70] Li S, Li J, He Y, Xu M, Zhang J, Du W, Zhao Y, Xia L . Precise gene replacement in rice by RNA transcript-templated homologous recombination. Nat Biotechnol, 2019, doi: 10.1038/s41587-019-0065-7.
[71] Zhao L, Deng L, Zhang Q, Jing X, Ma M, Yi B, Wen J, Ma C Z, Tu J X, Fu T D, Shen J X . Autophagy contributes to sulfonylurea herbicide tolerance via GCN2-independent regulation of amino acid homeostasis. Autophagy, 2018,14:702-714.
[72] Zhao L, Jing X, Chen L, Liu Y J, Su Y N, Liu T T, Gao C B, Yi B, Wen J, Ma C Z, Tu J, Zou J, Fu T D, Shen J X . Tribenuron- methyl induces male sterility through anther-specific inhibition of acetolactate synthase leading to autophagic cell death. Mol Plant, 2015,8:1710-1724.
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