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RESEARCH ARTICLE

Rapid mapping of a chlorina mutant gene cn-A1 in hexaploid wheat by bulked segregant analysis and single nucleotide polymorphism genotyping arrays

H. B. Jiang A , N. Wang A , J. T. Jian B , C. S. Wang A and Y. Z. Xie https://orcid.org/0000-0001-9584-3286 A C
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling 712100, China.

B Nanyang Academy of Agricultural Science, Henan 473000, China.

C Corresponding author. Email: Yanzhouxie@126.com

Crop and Pasture Science 70(10) 827-836 https://doi.org/10.1071/CP19165
Submitted: 18 April 2019  Accepted: 1 July 2019   Published: 25 October 2019

Abstract

The yellow–green leaf mutant can be exploited in photosynthesis and plant development research. A Triticum aestivum mutant with the chlorina phenotype, here called B23, was produced by treatment with the chemical mutagen sodium azide. This B23 mutant showed significantly lower chlorophyll content than wild-type Saannong33, and its chloroplast structure was abnormal. All its yield-related traits, except for the number of spikes per plant, were also significantly decreased. Genetic analysis confirmed that the mutant phenotype was controlled by a recessive gene, here designated cn-A1. Using bulked segregant analysis and the wheat 660K single nucleotide polymorphism array, the cn-A1 gene was mapped to chromosome 7AL, and 11 polymorphic markers were developed. Further analysis showed that cn-A1 was located in a 1.1-cM genetic region flanked by Kompetitive allele specific PCR (KASP) markers 660K-7A12 and 660K-7A20, which corresponded to a physical interval of 3.48 Mb in T. aestivum cv. Chinese Spring chromosome 7AL containing 47 predicted genes with high confidence. These results are expected to accelerate the process of cloning the cn-A1 gene and facilitate understanding of the mechanisms underlying chlorophyll metabolism and chloroplast development in wheat.

Additional keywords: Kompetitive allele specific PCR (KASP) markers, Triticum aestivum.


References

Ansari MJ, Al-Ghamdi A, Kumar R, Usmani S, Al-Attal Y, Nuru A, Mohamed AA, Singh K, Dhaliwal HS (2013) Characterization and gene mapping of a chlorophyll-deficient mutant clm1 of Triticum monococcum L. Biologia Plantarum 57, 442–448.
Characterization and gene mapping of a chlorophyll-deficient mutant clm1 of Triticum monococcum L.Crossref | GoogleScholarGoogle Scholar |

Avni R, Nave M, Barad O, Baruch K, Twardziok SO, Gundlach H, Hale I, Mascher M, Spannagl M, Wiebe K, Jordan KW, Golan G, Deek J, Ben-Zvi B, Ben-Zvi G, Himmelbach A, MacLachlan RP, Sharpe AG, Fritz A, Ben-David R, Budak H, Fahima T, Korol A, Faris JD, Hernandez A, Mikel MA, Levy AA, Steffenson B, Maccaferri M, Tuberosa R, Cattivelli L, Faccioli P, Ceriotti A, Kashkush K, Pourkheirandish M, Komatsuda T, Eilam T, Sela H, Sharon A, Ohad N, Chamovitz DA, Mayer KFX, Stein N, Ronen G, Peleg Z, Pozniak CJ, Akhunov ED, Distelfeld A (2017) Wild emmer genome architecture and diversity elucidate wheat evolution and domestication. Science 357, 93–97.
Wild emmer genome architecture and diversity elucidate wheat evolution and domestication.Crossref | GoogleScholarGoogle Scholar | 28684525PubMed |

Bossmann B, Knoetzel J, Jansson S (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynthesis Research 52, 127–136.
Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins.Crossref | GoogleScholarGoogle Scholar |

Brestič M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji HM, Allakhverdiev SI (2015a) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynthesis Research 125, 151–166.
Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines.Crossref | GoogleScholarGoogle Scholar | 25648638PubMed |

Brestič M, Zivcak M, Datko M, Olsovska K, Sytar O, Shao H (2015b) Novel resistance mechanism of barley chlorina f104 antenna mutant against photoinhibition: possible role of new identified chloroplastic cpNrp protein. Theoretical and Experimental Plant Physiology 27, 75–85.
Novel resistance mechanism of barley chlorina f104 antenna mutant against photoinhibition: possible role of new identified chloroplastic cpNrp protein.Crossref | GoogleScholarGoogle Scholar |

Brestič M, Zivcak M, Kunderlikova K, Allakhverdiev SI (2016) High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Photosynthesis Research 130, 251–266.
High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines.Crossref | GoogleScholarGoogle Scholar | 27023107PubMed |

Campbell BW, Mani D, Curtin SJ, Slattery RA, Michno JM, Ort DR, Schaus PJ, Palmer RG, Orf JH, Stupar RM (2015) Identical substitutions in magnesium chelatase paralogs result in chlorophyll-deficient soybean mutants. G3: Genes, Genomes, Genetics 5, 123–131.
Identical substitutions in magnesium chelatase paralogs result in chlorophyll-deficient soybean mutants.Crossref | GoogleScholarGoogle Scholar |

Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proceedings of the National Academy of Sciences of the United States of America 110, 8057–8062.
Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars.Crossref | GoogleScholarGoogle Scholar | 23630259PubMed |

Chen C, He Z, Lu J, Li J, Ren Y, Ma C, Xia X (2016) Molecular mapping of stripe rust resistance gene YrJ22 in Chinese wheat cultivar Jimai 22. Molecular Breeding 36, 118
Molecular mapping of stripe rust resistance gene YrJ22 in Chinese wheat cultivar Jimai 22.Crossref | GoogleScholarGoogle Scholar |

Cui F, Zhang N, Fan XL, Zhang W, Zhao CH, Yang LJ, Pan RQ, Chen M, Han J, Zhao XQ, Ji J, Tong YP, Zhang HX, Jia JZ, Zhao GY, Li JM (2017) Utilization of a Wheat660K SNP array-derived high-density genetic map for high-resolution mapping of a major QTL for kernel number. Scientific Reports 7, 3788
Utilization of a Wheat660K SNP array-derived high-density genetic map for high-resolution mapping of a major QTL for kernel number.Crossref | GoogleScholarGoogle Scholar | 28630475PubMed |

Doyle JJT, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12, 13–15.

Falbel TG, Staehelin LA (1994) Characterization of a family of chlorophyll-deficient wheat (Triticum) and barley (Hordeum vulgare) mutants with defects in the magnesium-insertion step of chlorophyll biosynthesis. Plant Physiology 104, 639–648.
Characterization of a family of chlorophyll-deficient wheat (Triticum) and barley (Hordeum vulgare) mutants with defects in the magnesium-insertion step of chlorophyll biosynthesis.Crossref | GoogleScholarGoogle Scholar | 8159789PubMed |

Falbel TG, Meehl JB, Staehelin LA (1996) Severity of mutant phenotype in a series of chlorophyll-deficient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis. Plant Physiology 112, 821–832.
Severity of mutant phenotype in a series of chlorophyll-deficient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis.Crossref | GoogleScholarGoogle Scholar | 8883392PubMed |

Gao M, Hu L, Li Y, Weng Y (2016) The chlorophyll-deficient golden leaf mutation in cucumber is due to a single nucleotide substitution in CsChlI for magnesium chelatase I subunit. Theoretical and Applied Genetics 129, 1961–1973.
The chlorophyll-deficient golden leaf mutation in cucumber is due to a single nucleotide substitution in CsChlI for magnesium chelatase I subunit.Crossref | GoogleScholarGoogle Scholar | 27435733PubMed |

Hansson A, Kannangara CG, von Wettstein D, Hansson M (1999) Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase. Proceedings of the National Academy of Sciences of the United States of America 96, 1744–1749.
Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase.Crossref | GoogleScholarGoogle Scholar | 9990095PubMed |

Harrison MA, Nemson JA, Melis A (1993) Assembly and composition of the chlorophyll ab light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants. Photosynthesis Research 38, 141–151.
Assembly and composition of the chlorophyll ab light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants.Crossref | GoogleScholarGoogle Scholar | 24317910PubMed |

Huang YS, Li HM (2009) Arabidopsis CHLI2 can substitute for CHLI1. Plant Physiology 150, 636–645.
Arabidopsis CHLI2 can substitute for CHLI1.Crossref | GoogleScholarGoogle Scholar | 19363094PubMed |

International Wheat Genome Sequencing Consortium, et al. (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191
Shifting the limits in wheat research and breeding using a fully annotated reference genome.Crossref | GoogleScholarGoogle Scholar | 30262504PubMed |

Jarvis P, Dormann P, Peto CA, Lutes J, Benning C, Chory J (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proceedings of the National Academy of Sciences of the United States of America 97, 8175–8179.
Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant.Crossref | GoogleScholarGoogle Scholar | 10869420PubMed |

Jia M, Guan J, Zhai Z, Geng S, Zhang X, Mao L, Li A (2018) Wheat functional genomics in the era of next generation sequencing: an update. The Crop Journal 6, 7–14.
Wheat functional genomics in the era of next generation sequencing: an update.Crossref | GoogleScholarGoogle Scholar |

Jung KH, Hur J, Ryu CH, Choi Y, Chung YY, Miyao A, Hirochika H, An GH (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant & Cell Physiology 44, 463–472.
Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system.Crossref | GoogleScholarGoogle Scholar |

Klindworth DL, Williams ND, Duysen ME (1995) Genetic analysis of chlorina mutants of durum wheat. Crop Science 35, 431–436.
Genetic analysis of chlorina mutants of durum wheat.Crossref | GoogleScholarGoogle Scholar |

Kosambi DD (1943) The estimation of map distances from recombination values. Annals of Human Genetics 12, 172–175.

Kosuge K, Watanabe N, Kuboyama T (2011) Comparative genetic mapping of homoeologous genes for the chlorina phenotype in the genus Triticum. Euphytica 179, 257–263.
Comparative genetic mapping of homoeologous genes for the chlorina phenotype in the genus Triticum.Crossref | GoogleScholarGoogle Scholar |

Li N, Jia J, Xia C, Liu X, Kong X (2013) Characterization and mapping of novel chlorophyll deficient mutant genes in durum wheat. Breeding Science 63, 169–175.
Characterization and mapping of novel chlorophyll deficient mutant genes in durum wheat.Crossref | GoogleScholarGoogle Scholar | 23853511PubMed |

Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11, 591–592.
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.Crossref | GoogleScholarGoogle Scholar |

Liu RH, Meng JL (2003) MapDraw: a Microsoft Excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas 25, 317–321.

Liu X-p, Yang C, Han F-q, Fang Z-y, Yang L-m, Zhuang M, Lv H-h, Liu Y-m, Li Z-s, Zhang Y-y (2016) Genetics and fine mapping of a yellow–green leaf gene (ygl-1) in cabbage (Brassica oleracea var. capitata L.). Molecular Breeding 36, 82
Genetics and fine mapping of a yellow–green leaf gene (ygl-1) in cabbage (Brassica oleracea var. capitata L.).Crossref | GoogleScholarGoogle Scholar |

Masuda T (2008) Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynthesis Research 96, 121–143.
Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls.Crossref | GoogleScholarGoogle Scholar | 18273690PubMed |

Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proceedings of the National Academy of Sciences of the United States of America 88, 9828–9832.
Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations.Crossref | GoogleScholarGoogle Scholar | 1682921PubMed |

Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends in Plant Science 15, 488–498.
The cell biology of tetrapyrroles: a life and death struggle.Crossref | GoogleScholarGoogle Scholar | 20598625PubMed |

Pettigrew R, Driscoll C, Rienits K (1969) A spontaneous chlorophyll mutant in hexaploid wheat. Heredity 24, 481
A spontaneous chlorophyll mutant in hexaploid wheat.Crossref | GoogleScholarGoogle Scholar |

Preiss S, Thornber JP (1995) Stability of the apoproteins of light-harvesting complex I and II during biogenesis of thylakoids in the chlorophyll b-less barley mutant Chlorina f2. Plant Physiology 107, 709–717.
Stability of the apoproteins of light-harvesting complex I and II during biogenesis of thylakoids in the chlorophyll b-less barley mutant Chlorina f2.Crossref | GoogleScholarGoogle Scholar | 12228395PubMed |

Qin D, Dong J, Xu F, Guo G, Ge S, Xu Q, Xu Y, Li M (2015) Characterization and fine mapping of a novel barley stage green-revertible albino gene (HvSGRA) by bulked segregant analysis based on SSR assay and specific length amplified fragment sequencing. BMC Genomics 16, 838
Characterization and fine mapping of a novel barley stage green-revertible albino gene (HvSGRA) by bulked segregant analysis based on SSR assay and specific length amplified fragment sequencing.Crossref | GoogleScholarGoogle Scholar | 26494145PubMed |

Qureshi N, Bariana H, Forrest K, Hayden M, Keller B, Wicker T, Faris J, Salina E, Bansal U (2017) Fine mapping of the chromosome 5B region carrying closely linked rust resistance genes Yr47 and Lr52 in wheat. Theoretical and Applied Genetics 130, 495–504.
Fine mapping of the chromosome 5B region carrying closely linked rust resistance genes Yr47 and Lr52 in wheat.Crossref | GoogleScholarGoogle Scholar | 27866228PubMed |

Ramirez-Gonzalez RH, Uauy C, Caccamo M (2015) PolyMarker: a fast polyploid primer design pipeline. Bioinformatics 31, 2038–2039.
PolyMarker: a fast polyploid primer design pipeline.Crossref | GoogleScholarGoogle Scholar | 25649618PubMed |

Rassadina VV, Averina NG, Koval SF (2005) Disturbance of chlorophyll formation at the level of 5-aminolevulinic acid and Mg-containing porphyrin synthesis in isogenic lines of spring wheat (Triticum aestivum L.) marked with genes cn-A1 and cn-D1. Doklady Biological Sciences 405, 472–473.
Disturbance of chlorophyll formation at the level of 5-aminolevulinic acid and Mg-containing porphyrin synthesis in isogenic lines of spring wheat (Triticum aestivum L.) marked with genes cn-A1 and cn-D1.Crossref | GoogleScholarGoogle Scholar | 16485648PubMed |

Sawers RJ, Viney J, Farmer PR, Bussey RR, Olsefski G, Anufrikova K, Hunter CN, Brutnell TP (2006) The maize Oil yellow 1 (Oy1) gene encodes the I subunit of magnesium chelatase. Plant Molecular Biology 60, 95–106.
The maize Oil yellow 1 (Oy1) gene encodes the I subunit of magnesium chelatase.Crossref | GoogleScholarGoogle Scholar | 16463102PubMed |

Sears LM, Sears ER (1968) The mutants Chlorina-1 and Hermsen’s Virescent. In ‘Proceedings of the 3rd International Wheat Genetics Symposium’. (Eds KW Finlay, KW Shepherd) pp. 299–304. (Australian Academy of Sciences: Canberra)

Semagn K, Babu R, Hearne S, Olsen M (2014) Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement. Molecular Breeding 33, 1–14.
Single nucleotide polymorphism genotyping using Kompetitive Allele Specific PCR (KASP): overview of the technology and its application in crop improvement.Crossref | GoogleScholarGoogle Scholar |

Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics 109, 1105–1114.
A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 15490101PubMed |

Stenbaek A, Jensen PE (2010) Redox regulation of chlorophyll biosynthesis. Phytochemistry 71, 853–859.
Redox regulation of chlorophyll biosynthesis.Crossref | GoogleScholarGoogle Scholar | 20417532PubMed |

Tripathy BC, Pattanayak GK (2012) Chlorophyll biosynthesis in higher plants. In ‘Photosynthesis: plastid biology, energy conversion and carbon assimilation’. (Eds JJ Eaton-Rye, BC Tripathy, TD Sharkey) pp. 63–94. (Springer: Dordrecht)

Van Ooijen J (2006) ‘JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations.’ (Kyazma BV: Wageningen)

Wang S, Wong D, Forrest K, Allen A, Chao S, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, International Wheat Genome Sequencing Lillemo M, Mather D, Appels R, Dolferus R, Brown , Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo MC, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnology Journal 12, 787–796.
Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array.Crossref | GoogleScholarGoogle Scholar | 24646323PubMed |

Wang Y, Xie J, Zhang H, Guo B, Ning S, Chen Y, Lu P, Wu Q, Li M, Zhang D, Guo G, Zhang Y, Liu D, Zou S, Tang J, Zhao H, Wang X, Li J, Yang W, Cao T, Yin G, Liu Z (2017) Mapping stripe rust resistance gene YrZH22 in Chinese wheat cultivar Zhoumai 22 by bulked segregant RNA-Seq (BSR-Seq) and comparative genomics analyses. Theoretical and Applied Genetics 130, 2191–2201.
Mapping stripe rust resistance gene YrZH22 in Chinese wheat cultivar Zhoumai 22 by bulked segregant RNA-Seq (BSR-Seq) and comparative genomics analyses.Crossref | GoogleScholarGoogle Scholar | 28711956PubMed |

Washington W, Sears E (1970) Ethyl methanesulfonate-induced chlorophyll mutations in Triticum aestivum. Canadian Journal of Genetics and Cytology 12, 851–859.
Ethyl methanesulfonate-induced chlorophyll mutations in Triticum aestivum.Crossref | GoogleScholarGoogle Scholar |

Watanabe N, Koval SE (2003) Mapping of chlorina mutant genes on the long arm of homoeologous group 7 chromosomes in common wheat with partial deletion lines. Euphytica 129, 259–265.
Mapping of chlorina mutant genes on the long arm of homoeologous group 7 chromosomes in common wheat with partial deletion lines.Crossref | GoogleScholarGoogle Scholar |

Wu Z, Zhang X, He B, Diao L, Sheng S, Wang J, Guo X, Su N, Wang L, Jiang L, Wang C, Zhai H, Wan J (2007) A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiology 145, 29–40.
A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis.Crossref | GoogleScholarGoogle Scholar | 17535821PubMed |

Wu J, Liu S, Wang Q, Zeng Q, Mu J, Huang S, Yu S, Han D, Kang Z (2018) Rapid identification of an adult plant stripe rust resistance gene in hexaploid wheat by high-throughput SNP array genotyping of pooled extremes. Theoretical and Applied Genetics 131, 43–58.
Rapid identification of an adult plant stripe rust resistance gene in hexaploid wheat by high-throughput SNP array genotyping of pooled extremes.Crossref | GoogleScholarGoogle Scholar | 28965125PubMed |

Xie YZ, Hong DF, Xu ZH, Liu PW, Yang GS (2008) Identification of AFLP markers linked to the epistatic suppressor gene of a recessive genic male sterility in rapeseed and conversion to SCAR markers. Plant Breeding 127, 145–149.
Identification of AFLP markers linked to the epistatic suppressor gene of a recessive genic male sterility in rapeseed and conversion to SCAR markers.Crossref | GoogleScholarGoogle Scholar |

Yamazaki J (2010) Changes in the photosynthetic characteristics and photosystem stoichiometries in wild-type and Chl b-deficient mutant rice seedlings under various irradiances. Photosynthetica 48, 521–529.
Changes in the photosynthetic characteristics and photosystem stoichiometries in wild-type and Chl b-deficient mutant rice seedlings under various irradiances.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Li J, Yoo JH, Yoo SC, Cho SH, Koh HJ, Seo HS, Paek NC (2006) Rice Chlorina-1 and Chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Molecular Biology 62, 325–337.
Rice Chlorina-1 and Chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development.Crossref | GoogleScholarGoogle Scholar | 16915519PubMed |

Zhang H, Zhang D, Han S, Zhang X, Yu D (2011) Identification and gene mapping of a soybean chlorophyll-deficient mutant. Plant Breeding 130, 133–138.
Identification and gene mapping of a soybean chlorophyll-deficient mutant.Crossref | GoogleScholarGoogle Scholar |

Zhang L, Liu C, An X, Wu H, Feng Y, Wang H, Sun D (2017) Identification and genetic mapping of a novel incompletely dominant yellow leaf color gene, Y1718, on chromosome 2BS in wheat. Euphytica 213, 141
Identification and genetic mapping of a novel incompletely dominant yellow leaf color gene, Y1718, on chromosome 2BS in wheat.Crossref | GoogleScholarGoogle Scholar |

Zhu J, Chen J, Gao F, Xu C, Wu H, Chen K, Si Z, Yan H, Zhang T (2017) Rapid mapping and cloning of the virescent-1 gene in cotton by bulked segregant analysis–next generation sequencing and virus-induced gene silencing strategies. Journal of Experimental Botany 68, 4125–4135.
Rapid mapping and cloning of the virescent-1 gene in cotton by bulked segregant analysis–next generation sequencing and virus-induced gene silencing strategies.Crossref | GoogleScholarGoogle Scholar | 28922761PubMed |

Zivcak M, Brestic M, Botyanszka L, Chen YE, Allakhverdiev SI (2019) Phenotyping of isogenic chlorophyll-less bread and durum wheat mutant lines in relation to photoprotection and photosynthetic capacity. Photosynthesis Research 139, 239–251.
Phenotyping of isogenic chlorophyll-less bread and durum wheat mutant lines in relation to photoprotection and photosynthetic capacity.Crossref | GoogleScholarGoogle Scholar | 30019176PubMed |