Abstract
Main conclusion
This study confirms a high level of metabolic resistance to the herbicide chlorsulfuron, inherited by a single dominant gene in a sorghum genotype (GL-1).
Abstract
Chlorsulfuron, an acetolactate synthase (ALS)-inhibitor, effectively controls post-emergence grass and broadleaf weeds but is not registered for use in sorghum because of crop injury. The objectives of this study were to characterize the inheritance and mechanism of chlorsulfuron resistance in the sorghum genotype GL-1. Chlorsulfuron dose–response experiments were conducted using GL-1 along with BTx623 (susceptible check), and Pioneer 84G62 (commercial sorghum hybrid). The F1 and F2 progeny were generated by crossing GL-1 with BTx623. To assess if the target site alterations bestow resistance, the ALS gene, the molecular target of chlorsulfuron, was sequenced from GL-1. The role of cytochrome P450 (CYP) in metabolizing chlorsulfuron, using malathion, a CYP-inhibitor was tested. The chlorsulfuron dose–response assay indicated that GL-1 and F1 progeny were ~ 20-fold more resistant to chlorsulfuron relative to BTx623. The F2 progenies segregated 3:1 (resistance: susceptibility) suggesting that chlorsulfuron resistance in GL-1 is a single dominant trait. No mutations in the ALS gene were detected in the GL-1; however, a significant reduction in biomass accumulation was found in plants pre-treated with malathion indicating that metabolism of chlorsulfuron contributes to resistance in GL-1. Also, GL-1 is highly susceptible to other herbicides (e.g., mesotrione and tembotrione) compared to Pioneer 84G62, suggesting the existence of a negative cross-resistance in GL-1. Overall, these results confirm a high level of metabolic resistance to chlorsulfuron inherited by a single dominant gene in GL-1 sorghum. These results have potential for developing chlorsulfuron-tolerant sorghum hybrids, with the ability to improve post-emergence weed control.
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Abbreviations
- ALS:
-
Acetolactate synthase
- CYP:
-
Cytochrome P450
- HPPD:
-
4-Hydroxyphenylpyruvate dioxygenase
- IMI:
-
Imidazolinone
- POST:
-
Postemergence
- SU:
-
Sulfonylurea
- WAT:
-
Weeks after treatment
References
Abusin RMA, Eltayeb AH, Hassan MM, Babiker AGT (2017) Integrated management of Striga hermonthica on sorghum. Asian J Adv Agric Res 4(2):1–8. https://doi.org/10.9734/AJAAR/2017/38141
Baerg RJ, Barrett M, Polge ND (1996) Insecticide and insecticide metabolite interactions with cytochrome P450 mediated activities in maize. Pestic Biochem Physiol 55:10–20. https://doi.org/10.1006/pest.1996.0030
Beckie HJ, Johnson EN, Légère A (2012) Negative cross-resistance of acetolactate synthase inhibitor–resistant kochia (Kochia scoparia) to protoporphyrinogen oxidase–and hydroxyphenylpyruvate dioxygenase–inhibiting herbicides. Weed Technol 26:570–574. https://doi.org/10.1614/WT-D-12-00020.1
Bolwell GP, Bozak K, Zimmerlin A (1994) Plant cytochrome P450. Phytochemistry 37:1491–1506. https://doi.org/10.1016/s0031-9422(00)89567-9
Busi R, Vila-Aiub MM, Powles SB (2011) Genetic control of a cytochrome P450 metabolism-based herbicide resistance mechanism in Lolium rigidum. Heredity 106:817–824. https://doi.org/10.1038/hdy.2010.124
Casa AM, Pressoir G, Brown PJ, Mitchell SE, Rooney WL, Tuinstra MR, Franks CD, Kresovich S (2008) Community resources and strategies for association mapping in sorghum. Crop Sci 48:30–40. https://doi.org/10.2135/cropsci2007.02.0080
Christopher JT, Preston C, Powles SB (1994) Malathion antagonizes metabolism-based chlorsulfuron resistance in Lolium rigidum. Pestic Biochem Physiol 49:172–182. https://doi.org/10.1006/pest.1994.1045
Ciampitti IA, Prasad PVV (2019) Sorghum: state of the art and future perspectives Agronomy Monograph 58. American Society of Agronomy, Madison, WI, USA
Cink JH (1986) Interaction of two sulfonylurea herbicides with selected insecticides on wheat. Oklahoma State University, USA
Cochran WG (1952) The χ2 test of goodness of fit. Ann Math Stat 1:315–345
De Mendiburu F (2014) Agricolae: statistical procedures for agricultural research. R package version 1.1. https://tarwi.lamolina.edu.pe/~fmendiburu/indexfiler/download/ENagricolae.pdf
De Prado R, Sanchez M, Jorrin J, Dominguez C (1992) Negative cross-resistance to bentazone and pyridate in atrazine resistant Amaranthus cruentus and Amaranthus hybridus biotypes. Pestic Sci 35:131–136. https://doi.org/10.1002/ps.2780350206
Deng W, Cao Y, Yang Q, Liu JM, Mei Y, Zheng M (2014) Different cross-resistance patterns to AHAS herbicides of two tribenuron-methyl resistant flixweed (Descurainia sophia L.) biotypes in China. Pestic Biochem Physiol 112:26–32. https://doi.org/10.1016/j.pestbp.2014.05.003
Development Core Team (2013) R: A language and environment for statistical computing. https://www.r-project.org/contributors.html
Devine MD, Shukla A (2000) Altered target sites as a mechanism of herbicide resistance. Crop Prot 19:881–889. https://doi.org/10.1016/S0261-2194(00)00123-X
Dille JA, Stahlman PW, Thompson CR, Bean BW (2020) Potential yield loss in grain sorghum (Sorghum bicolor) with weed interference in the United States. Weed Technol 34:624–629. https://doi.org/10.1017/wet.2020.12
Ferreira KL, Baker TK, Peeper TF (1990) Factors influencing winter wheat (Triticum aestivum) injury from sulfonylurea herbicides. Weed Technol 4:724–730. https://doi.org/10.1017/S0890037X00026294
Gadamski G, Ciarka D, Gressel J, Gawronski SW (2000) Negative cross-resistance in triazine-resistant biotypes of Echinochloa crus-galli and Conyza canadensis. Weed Sci 48:176–180. https://doi.org/10.1614/0043-1745(2000)048[0176:NCRITR]2.0.CO;2
Gaines TA, Shaner DL, Dayan FE (2018) Introduction to pest management science special issue for GHRC 2017. Pest Manag Sci 74:2209–2210. https://doi.org/10.1002/ps.5128
Gressel J, Segel LA (1990) Negative cross resistance; a possible key to atrazine resistance management: a call for whole plant data. Z Naturforschung C 45:470–473
Hageman LH, Behrens R (1981) Response of small-grain cultivars to chlorsulfuron. Weed Sci 29:414–420. https://doi.org/10.1017/S0043174500039928
Han H, Yu Q, Vila-Aiub M, Powles SB (2014) Genetic inheritance of cytochrome P450-mediated metabolic resistance to chlorsulfuron in a multiple herbicide resistant Lolium rigidum population. Crop Prot 65:57–63. https://doi.org/10.1016/j.cropro.2014.06.026
Hatzios KK (1984) Potential safeners for protecting sorghum (Sorghum bicolor (L.) Moench) against chlorsulfuron, fluazifop-butyl and sethoxydim. Weed Res 24:249–254
Heap I (2020) The International Herbicide-Resistant Weed Database. www.weedscience.org. (Accessed 10 May 2020)
Hennigh SD, Al-Khatib K, Tuinstra MR (2010) Postemergence weed control in acetolactate synthase–resistant grain sorghum. Weed Technol 24:219–225. https://doi.org/10.1614/WT-D-09-00014.1
Jugulam M, Shyam C (2019) Non-target-site resistance to herbicides: recent developments. Plants 8:417. https://doi.org/10.3390/plants8100417
Kaspar M, Grondona M, Leon A, Zambelli A (2011) Selection of a sunflower line with multiple herbicide tolerance that is reversed by the P450 inhibitor malathion. Weed Sci 59:232–237. https://doi.org/10.1614/WS-D-10-00120.1
Kershner KS (2010) Herbicide resistance in grain sorghum. Kansas State University, USA
Knezevic SZ, Streibig JC, Ritz C (2007) Utilizing R software package for dose-response studies: the concept and data analysis. Weed Technol 21:840–848. https://doi.org/10.1614/WT-06-161.1
Kreuz K, Fonné-Pfister R (1992) Herbicide-insecticide interaction in maize: malathion inhibits cytochrome P450-dependent primisulfuron metabolism. Pestic Biochem Physiol 43:232–240. https://doi.org/10.1016/0048-3575(92)90036-Y
Landi P, Frascaroli E, Vicari A (1990) Inheritance of chlorsulfuron tolerance in a maize population. J Genet Breed 44:27–32
Leetch MS (1985) Evaluation of chlorsulfuron for weed control in winter wheat (Triticum aestivum L.) and its effect on subsequent recropping with soybeans (Glycine max (L.) Merr.) or grain sorghum (Sorghum bicolor (L.) Moench). Kansas State University, USA
Liu X, Bi B, Xu X, Li B, Tian S, Wang J, Zhang H, Wang G, McElroy JS (2019) Rapid identification of a candidate nicosulfuron sensitivity gene (Nss) in maize (Zea mays L.) via combining bulked segregant analysis and RNA-seq. Theor Appl Genet 132:1351–1361. https://doi.org/10.1007/s00122-019-03282-8
Lopez-Martinez N, Marshall G, De Prado R (1997) Resistance of barnyard grass (Echinochloa crus-galli) to atrazine and quinclorac. Pestic Sci 51:171–175
Nakka S, Thompson CR, Peterson DE, Jugulam M (2017) Target site–based and non–target site-based resistance to ALS inhibitors in palmer amaranth (Amaranthus palmeri). Weed Sci 65:681–689. https://doi.org/10.1017/wsc.2017.43
Ohadi S, Hodnett G, Rooney W, Bagavathiannan M (2017) Gene flow and its consequences in sorghum spp. CRC Crit Rev Plant Sci 36:367–385. https://doi.org/10.1080/07352689.2018.1446813
Oliveira MC, Gaines TA, Dayan FE, Patterson EL, Jhala AJ, Knezevic SZ (2018) Reversing resistance to tembotrione in an Amaranthus tuberculatus (var. rudis) population from Nebraska, USA with cytochrome P450 inhibitors. Pest Manag Sci 74:2296–2305. https://doi.org/10.1002/ps.4697
Pandian BA, Varanasi A, Vennapusa AR, Sathishraj R, Lin G, Zhao M, Tunnell M, Tesso T, Liu S, Vara Prasad PV, Jugulam M (2020) Characterization, genetic analyses, and identification of QTLs conferring metabolic resistance to a 4-hydroxyphenylpyruvate dioxygenase-inhibitor in sorghum (Sorghum bicolor). Front Plant Sci 11:1890. https://doi.org/10.3389/fpls.2020.596581
Peterson MA, Arnold WE (1986) Response of rotational crops to soil residues of chlorsulfuron. Weed Sci 34:131–136. https://doi.org/10.1017/S004317450002659X
Petit C, Duhieu B, Boucansaud K, Délye C (2010) Complex genetic control of non-target-site-based resistance to herbicides inhibiting acetyl-coenzyme A carboxylase and acetolactate-synthase in Alopecurus myosuroides Huds. Plant Sci 178:501–509. https://doi.org/10.1016/j.plantsci.2010.03.007
Preston C, Malone JM (2015) Inheritance of resistance to 2, 4-D and chlorsulfuron in a multiple-resistant population of Sisymbrium orientale. Pest Manag Sci 71:1523–1528
Puri A, Haller WT, Netherland MD (2009) Cross-resistance in fluridone-resistant hydrilla to other bleaching herbicides. Weed Sci 57:482–488. https://doi.org/10.1614/WS-09-060.1
Rakshit S, Bellundagi A (2019) Chapter 5 - Conventional breeding techniques in sorghum. In: Aruna C, Visarada KBRS, Bhat BV, Tonapi VA (eds) Breeding sorghum for diverse end uses. Woodhead Publishing, Duxford, UK, pp 77–91
Ray TB (1984) Site of action of chlorsulfuron: inhibition of valine and isoleucine biosynthesis in plants. Plant Physiol 75:827–831. https://doi.org/10.1104/pp.75.3.827
Reddy PS, Kumar AA (2008) Emasculation and selfing techniques in sorghum. In: Reddy BVS, Ramesh S, Ashok Kumar A, Gowda CLL (eds) Sorghum improvement in the new millennium. International Crops Research Institute for the Semi-Arid Tropics, Andhra Pradesh
Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22
Russel MH, Saladini JL, Lichtner F (2002) Sulfonylurea herbicides. Pestic Outlook 13:166–173
Scarabel L, Carraro N, Sattin M, Varotto S (2004) Molecular basis and genetic characterisation of evolved resistance to ALS-inhibitors in Papaver rhoeas. Plant Sci 166:703–709. https://doi.org/10.1016/j.plantsci.2003.11.006
Sharma R, Pahuja SS, Balyan RS, Malik RK (2002) Effect of sulfonylurea herbicides applied alone and tank mix with metribuzin on weeds in wheat and their residual effect on succeeding crop of sorghum. Indian J Weed Sci 34:178–183
Shimizu T, Kaku K, Kawai K, Miyazawa T, Tanaka Y (2005) Molecular characterization of acetolactate synthase in resistant weeds and crops. In: Clark JM, Ohkawa H (eds) Environmental fate and safety management of agrochemicals. American Chemical Society, DC, USA, pp 255–271
Shyam C, Jhala AJ, Kruger G, Jugulam M (2019) Rapid metabolism increases the level of 2,4-D resistance at high temperature in common waterhemp (Amaranthus tuberculatus). Sci Rep 9:16695. https://doi.org/10.1038/s41598-019-53164-8
Siminszky B (2006) Plant cytochrome P450-mediated herbicide metabolism. Phytochem Rev 5:445–458. https://doi.org/10.1007/s11101-006-9011-7
Smith K, Scott B, Espinoza L, Kelley J (2010) Weed control in grain sorghum. In: Espinoza L, Kelley J (eds) Grain sorghum production handbook. Cooperative extension service University of Arkansas, Little Rock, AR, USA, pp 47–49
Stahlman PW, Wicks GA, Smith CW, Frederiksen RA (2000) Weeds and their control in grain sorghum Sorghumorigin history technology and production. Wiley, NY
Sweetser PB, Schow GS, Hutchison JM (1982) Metabolism of chlorsulfuron by plants: Biological basis for selectivity of a new herbicide for cereals. Pestic Biochem Physiol 17:18–23. https://doi.org/10.1016/0048-3575(82)90121-3
Tan LR, Lu YC, Zhang JJ, Luo F, Yang H (2015) A collection of cytochrome P450 monooxygenase genes involved in modification and detoxification of herbicide atrazine in rice (Oryza sativa) plants. Ecotoxicol Environ Saf 119:25–34. https://doi.org/10.1016/j.ecoenv.2015.04.035
Tardif FJ, Powles SB (1999) Effect of malathion on resistance to soil-applied herbicides in a population of rigid ryegrass (Lolium rigidum). Weed Sci 47:258–261
Thompson CR, Thill DC, Mallory-Smith CA, Shafii B (1994) Characterization of chlorsulfuron resistant and susceptible kochia (Kochia scoparia). Weed Technol 8:470–476. https://doi.org/10.1017/S0890037X00039531
Thompson CR, Dille JA, Peterson DE (2019) Weed competition and management in sorghum. In: Ciampitti IA, Vara Prasad PV (eds) Sorghum: state of the art and future perspectives. American Society of Agronomy, Madison, WI
Thyssen GN, Naoumkina M, McCarty JC, Jenkins NJ, Florane C, Li P, Fang DD (2018) The P450 gene CYP749A16 is required for tolerance to the sulfonylurea herbicide trifloxysulfuron sodium in cotton (Gossypium hirsutum L.). BMC Plant Biol 18:186. https://doi.org/10.1186/s12870-018-1414-2
Tranel PJ, Wright TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:700–712. https://doi.org/10.1614/0043-1745(2002)050[0700:RROWTA]2.0.CO;2
Tuinstra MR, Al-Khatib K (2011) Acetolactate synthase herbicide resistant sorghum. US Patent Application No. 12/517,937. USDA-NASS (2020) https://www.nass.usda.gov/. (Accessed 12 May 2020)
Visarada K, Aruna C (2019) Sorghum: a bundle of opportunities in the 21st Century. In: Aruna C, Visarada KBRS, Bhat BV, Tonapi VA (eds) Breeding sorghum for diverse end uses. Woodhead Publishing, Duxford, UK, pp 1–14
Wen-Sheng X, Xiang-Jing W, Tian-Rui R, Su-Qin C (2006) Purification of recombinant wheat cytochrome P450 monooxygenase expressed in yeast and its properties. Protein Expr Purif 45:54–59. https://doi.org/10.1016/j.pep.2005.07.004
Werck-Reichhart D, Hehn A, Didierjean L (2000) Cytochromes P450 for engineering herbicide tolerance. Trends Plant Sci 5:116–123. https://doi.org/10.1016/s1360-1385(00)01567-3
Werle R, Begcy K, Yerka MK, Mower JP (2017a) Independent evolution of acetolactate synthase–inhibiting herbicide resistance in weedy sorghum populations across common geographic regions. Weed Sci 65:164–176. https://doi.org/10.1614/WS-D-16-00095.1
Werle R, Tenhumberg B, Lindquist JL (2017b) Modeling shattercane dynamics in herbicide-tolerant grain sorghum cropping systems. Ecol Modell 343:131–141. https://doi.org/10.1016/j.ecolmodel.2016.10.023
Wickham H, Wickham MH (2007) The ggplot package. http://ftp.uni-bayreuth.de/math/statlib/R/CRAN/doc/packages/ggplot.pdf. (Accessed 12 May 2020)
Xiang W, Wang X, Ren T (2006) Expression of a wheat cytochrome P450 monooxygenase cDNA in yeast catalyzes the metabolism of sulfonylurea herbicides. Pestic Biochem Physiol 85:1–6.https://doi.org/10.1016/j.pestbp.2005.09.001
Yu Q, Powles S (2014) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:1106–1118. https://doi.org/10.1104/pp.114.242750
Yu Q, Shane Friesen LJ, Zhang XQ, Powles SB (2004) Tolerance to acetolactate synthase and acetyl-coenzyme A carboxylase inhibiting herbicides in Vulpia bromoides is conferred by two co-existing resistance mechanisms. Pestic Biochem Physiol 78:21–30. https://doi.org/10.1016/j.pestbp.2003.07.004
Zhou Q, Liu W, Zhang Y, Liu KK (2007) Action mechanisms of acetolactate synthase-inhibiting herbicides. Pestic Biochem Physiol 89:89–96. https://doi.org/10.1016/j.pestbp.2007.04.004
Acknowledgements
Graduate student assistantship to Pandian from Kansas Grain Sorghum Commission and College of Agriculture, Kansas State University is highly appreciated. This is contribution number 20-289-J from the Kansas Agricultural Experiment Station, Kansas State University, Manhattan, KS 66506-5502, USA.
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Pandian, B.A., Sathishraj, R., Prasad, P.V.V. et al. A single gene inherited trait confers metabolic resistance to chlorsulfuron in grain sorghum (Sorghum bicolor). Planta 253, 48 (2021). https://doi.org/10.1007/s00425-020-03563-3
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DOI: https://doi.org/10.1007/s00425-020-03563-3