Abstract
Key message
A candidate nicosulfuron sensitivity gene Nss was identified by combining bulked segregant analysis and RNA-seq. Multiple mutations of this gene were discovered in nicosulfuron-sensitive maize compared with the tolerant.
Abstract
It has been demonstrated that variabilities exist in maize response to nicosulfuron. Two nicosulfuron-sensitive inbred lines (HB39, HB41) and two tolerant inbred lines (HB05, HB09) were identified via greenhouse and field trials. Genetic analysis indicated that the sensitivity to nicosulfuron in maize was controlled by a single, recessive gene. To precisely and rapidly map the nicosulfuron sensitivity gene (Nss), two independent F2 segregating populations, Population A (HB41 × HB09) and Population B (HB39 × HB05), were constructed. By applying bulked segregant RNA-Seq (BSR-Seq), the Nss gene was, respectively, mapped on the short arm of chromosome 5 (chr5: 1.1–15.3 Mb) and (chr5: 0.5–18.2 Mb) using two populations, with 14.2 Mb region in common. Further analysis revealed that there were 43 and 119 differentially expressed genes in the mapping intervals, with 18 genes in common. Gene annotation results showed that a cytochrome P450 gene (CYP81A9) appeared to be the candidate gene of Nss associated with nicosulfuron sensitivity in maize. Sequence analysis demonstrated that two common deletion mutations existed in the sensitive maize, which might lead to the nicosulfuron sensitivity in maize. The results will make valuable contributions to the understanding of molecular mechanism of herbicide sensitivity in maize.
Similar content being viewed by others
References
Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H et al (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178
Barrett M (1995) Metabolism of herbicides by cytochrome P450 in corn. Drug Metab Drug Interact 12:299–316
Bray NL, Pimentel H, Melsted P, Pachter L (2016) Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol 34:525–527
Cabello-Hurtado F, Batard Y, Salaün J-P, Durst F, Pinot F et al (1998) Cloning, expression in yeast, and functional characterization of CYP81B1, a plant cytochrome P450 that catalyzes in-chain hydroxylation of fatty acids. J Biol Chem 273:7260–7267
Chayut N, Yuan H, Ohali S, Meir A, Yeselson Y et al (2015) A bulk segregant transcriptome analysis reveals metabolic and cellular processes associated with Orange allelic variation and fruit β-carotene accumulation in melon fruit. BMC Plant Biol 15:274
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C et al (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70
Ferrero R, Lima M, Davis AS, Gonzalez-Andujar JL (2017) Weed diversity affects soybean and maize yield in a long term experiment in Michigan, USA. Front Plant Sci 8:236
Gallaher K, Mueller TC, Hayes RM, Schwartz O, Barrett M (1999) Absorption, translocation, and metabolism of primisulfuron and nicosulfuron in broadleaf signalgrass (Brachiaria platyphylla) and corn. Weed Sci 47:8–12
Green JM, Ulrich JF (1993) Response of corn (Zea mays L.) inbreds and hybrids to sulfonylurea herbicides. Weed Sci 41:508–516
Huang Z, Peng G, Liu X, Deora A, Falk KC et al (2017) Fine mapping of a clubroot resistance gene in Chinese cabbage using SNP markers identified from bulked segregant RNA sequencing. Front Plant Sci 8:1448
Iwakami S, Endo M, Saika H, Okuno J, Nakamura N et al (2014) Cytochrome P450 CYP81A12 and CYP81A21 are associated with resistance to two acetolactate synthase inhibitors in Echinochloa phyllopogon. Plant Physiol 165:618–629
Jerald KP, Michael DM, Joseph DB, Chris MB, Martin MW (2008) Genetic Basis for varied levels of injury to sweet corn hybrids from three cytochrome P450-metabolized herbicides. J Am Soc Hort Sci 133:438–447
Kang M (1993) Inheritance of susceptibility to nicosulfuron herbicide in maize. J Hered 84:216–217
Kim S, Kim C-W, Park M, Choi D (2015) Identification of candidate genes associated with fertility restoration of cytoplasmic male-sterility in onion (Allium cepa L.) using a combination of bulked segregant analysis and RNA-seq. Theor Appl Genet 128:2289–2299
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Li J, Yu H, Zhang F, Lin C, Gao J, Fang J, Ding X, Shen Z, Xu X (2013) A built-in strategy to mitigate transgene spreading from genetically modified corn. PLoS ONE 8(12):e81645
Li M, Li B, Guo G, Chen Y, Xie J et al (2018) Mapping a leaf senescence gene els1 by BSR-Seq in common wheat. Crop J 6:236–243
Liu C, Liu S, Wang F, Wang Y, Liu K (2012a) Expression of a rice CYP81A6 gene confers tolerance to bentazon and sulfonylurea herbicides in both Arabidopsis and tobacco. Plant Cell. Tissue Organ Cult (PCTOC) 109:419–428
Liu S, Yeh C-T, Tang HM, Nettleton D, Schnable PS (2012b) Gene mapping via bulked segregant RNA-Seq (BSR-Seq). PLoS ONE 7:e36406
Liu X, Xu X, Li B, Wang X, Wang G et al (2015) RNA-seq transcriptome analysis of maize inbred carrying nicosulfuron-tolerant and nicosulfuron-susceptible alleles. Int J Mol Sci 16:5975–5989
Liu XM, Xu X, Li BH, Yao XX, Zhang HH et al (2018) Genomic and transcriptomic insights into cytochrome P450 monooxygenase genes involved in nicosulfuron tolerance in maize (Zea mays L.). J Integr Agric 17:1790–1799
Massinga RA, Currie RS, Trooien TP (2003) Water use and light interception under Palmer amaranth (Amaranthus palmeri) and corn competition. Weed Sci 51:523–531
Meyer MD, Pataky JK, Williams MM (2010) Genetic factors influencing adverse effects of mesotrione and nicosulfuron on sweet corn yield. Agron J 102:1138–1144
Moreno OJ (1999) Chromosomal Location of Genes for Leafiness (Lfy1) and Susceptibility to Nicosulfuron (Nsf1) in Maize Genome. Dissertation, Louisiana State University
Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M et al (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342
Nelson D, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66:194–211
Nordby JN, Williams MM, Pataky JK, Riechers DE, Lutz JD (2008) A common genetic basis in sweet corn inbred Cr1 for cross sensitivity to multiple cytochrome P450-metabolized herbicides. Weed Sci 56:376–382
Pan G, Zhang X, Liu K, Zhang J, Wu X et al (2006) Map-based cloning of a novel rice cytochrome P450 gene CYP81A6 that confers resistance to two different classes of herbicides. Plant Mol Biol 61:933–943
Paporisch A, Rubin B (2017) Isoxadifen safening mechanism in sweet corn genotypes with differential response to P450-metabolized herbicides. Pestic Biochem Physiol 138:22–28
Pataky JK, Williams MM, Riechers DE, Meyer MD (2009) A common genetic basis for cross-sensitivity to mesotrione and nicosulfuron in sweet corn hybrid cultivars and inbreds grown throughout North America. J Am Soc Hortic Sci 134:252–260
Pimentel H, Bray NL, Puente S, Melsted P, Pachter L (2017) Differential analysis of RNA-seq incorporating quantification uncertainty. Nat Methods 14:687
Reiner A, Yekutieli D, Benjamini Y (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19:368–375
Siminszky B (2006) Plant cytochrome P450-mediated herbicide metabolism. Phytochem Rev 5:445–458
Sprague CL, Penner D, Kells JJ (1999) Physiological basis for tolerance of four Zea mays hybrids to RPA 201772. Weed Sci 47:631–635
Sun L, Wu R, Su W, Gao Z, Lu C (2017) Physiological basis for isoxadifen-ethyl induction of nicosulfuron detoxification in maize hybrids. PLoS ONE 12:e0173502
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Wang J, Zhong X, Li F, Shi Z (2018) Effects of nicosulfuron on growth, oxidative damage, and the ascorbate-glutathione pathway in paired nearly isogenic lines of waxy maize (Zea mays L.). Pestic Biochem Physiol 145:108–117
Werck-Reichhart D, Hehn A, Didierjean L (2000) Cytochromes P450 for engineering herbicide tolerance. Trends Plant Sci 5:116–123
Williams MM, Pataky JK, Nordby JN, Riechers DE, Sprague CL et al (2005) Cross-sensitivity in sweet corn to nicosulfuron and mesotrione applied postemergence. HortScience 40:1801–1805
Williams M, Sowinski S, Dam T, Li BL (2006). Map-based cloning of the nsf1 gene of maize. In: 48th Maize genetics conference, p 49
Wu P, Xie J, Hu J, Qiu D, Liu Z et al (2018) Development of molecular markers linked to powdery mildew resistance gene Pm4b by combining SNP discovery from transcriptome sequencing data with bulked segregant analysis (BSR-Seq) in wheat. Front Plant Sci 9:95
Yamada T, Kambara Y, Imaishi H, Ohkawa H (2000) Molecular cloning of novel cytochrome P450 species induced by chemical treatments in cultured tobacco cells. Pestic Biochem Physiol 68:11–25
Acknowledgements
This research was financially supported by the National Natural Science Foundation of China (31501660), the National Key R&D Program of China (2018YFD0200600) and the Technology Research and Development Program of Hebei, China (17226507D).
Author information
Authors and Affiliations
Contributions
Author contribution statement
XL and GW designed the experiments and drafted the manuscript; XL, BB, XX and HZ carried out the experiments and analysis of RNA-seq; BL, ST and JW carried out the phenotyping; GW, YH and JSM conceived the idea of the study and finalized the manuscript. All of the authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Michael Gore.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Liu, X., Bi, B., Xu, X. et al. 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 (2019). https://doi.org/10.1007/s00122-019-03282-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03282-8