Abstract
Key message
We cloned and developed functional markers for the SiCHLI gene, which is responsible for the yellow–green color of leaves in foxtail millet, a frequently used marker trait in the hybrid breeding of foxtail millet by using bulked segregant analysis sequencing and haplotype analysis on the F2 and core-collected nature populations.
Abstract
The color of leaves has been widely used as a marker for the hybrid breeding of foxtail millet; however, few related gene have been cloned to date. Here, we used two F2 populations generated from crosses between the highly male-sterile material 125A with yellow–green leaves, and CG58 and S410, which have green leaves, to identify the genes underlying the yellow–green color of the leaves of foxtail millet. The leaves of 125A seedlings were yellow–green, but they became green at the heading stage. The content of chlorophyll a and chlorophyll b was lower, the number of thylakoid lamellae and grana was reduced, and the chloroplasts was more rounded in 125A than in S410 at the yellow–green leaf stage; however, no differences were observed between 125A and S410 in these traits and photosynthetic at the heading stage. Bulked segregant analysis and map-based cloning revealed that the SiCHLI gene is responsible for the leaf colors of 125A. A nonsynonymous mutation (C/T) in exon 3 causes yellow–green leaves in 125A at the seedling stage. Haplotype analysis of the SiCHLI gene in 596 core collected accessions revealed a new haplotype associated with high photosynthetic metabolic potential at the heading and mature stages, which could be used to enhance sterile lines with yellow–green leaves. We developed a functional marker that will facilitate the identification of foxtail millet accessions with the different types of yellow–green leaves. Generally, our study provides new genetic resources to guide the future marker-assisted or target-base editing in foxtail millet hybrid breeding.
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Data availability
The re-sequenced NGS data, used in this study, were uploaded to the National Center for Biotechnology Information BioProject database under the accession number PRJNA809753.
Change history
23 March 2023
A Correction to this paper has been published: https://doi.org/10.1007/s00122-023-04323-z
References
Beale SI (2005) Green genes gleaned. Trends Plant Sci 10:309–312
Bettinger R, Barton L, Morgan C (2010) The origins of food production in North China: a different kind of agricultural revolution. Evol Anthropol 19:9–21. https://doi.org/10.1002/evan.20236
Binhua H, Ping W, Anping D, Hui L, Minxia W, Yulu B, Zhandong J, Zhigang P (2021) Characterization and gene mapping of pyl3 mutant in rice. J Nucl Agric Sci 35:2696–2703
Brutnell T, Wang L, Swartwood K, Goldschmidt A, Jackson D, Zhu X, Kellogg E, Van Eck J (2010) Setaria viridis: a model for C4 photosynthesis. Plant Cell 22:2537–2544. https://doi.org/10.1105/tpc.110.075309
Chai L, Feng B, Liu X, Jiang L, Yuan S, Zhang Z, Li H, Zhang J, Fernando D, Xu C, Cui C, Jiang J, Zheng B, Wu L (2021) Fine mapping of a locus underlying the ectopic blade-like outgrowths on leaf and screening Its candidate genes in rapeseed (Brassica napus L.). Front Plant Sci. https://doi.org/10.3389/fpls.2020.616844
Deng X, Zhang H, Wang Y, He F, Liu J, Xiao X, Shu Z, Li W, Wang G, Wang G (2014) Mapped clone and functional analysis of leaf-color gene Ygl7 in a rice hybrid (Oryza sativa L. ssp. indica). PLoS ONE 9:e99564. https://doi.org/10.1371/journal.pone.0099564
Diao X, Schnable J, Bennetzen JL, Li J (2014) Initiation of Setaria as a model plant. Front Agric Sci Eng 1:16–20
Doust A, Diao X (2017) Genetics and genomics of Setaria. Springer
Du H, Qi M, Cui X, Cui Y, Yang H, Zhang J, Ma Y, Zhang S, Zhang X, Yu D (2018) Proteomic and functional analysis of soybean chlorophyll-deficient mutant cd1 and the underlying gene encoding the CHLI subunit of Mg-chelatase. Mol Breed 38:1–14
Doust AN, Kellogg EA, Devos KM, Bennetzen JL (2009) Foxtail millet: a sequence-driven grass model system. Plant Physiol 149:137–141
Gou X, Feng X, Shi H, Guo T, Xie R, Liu Y, Wang Q, Li H, Yang B, Chen L, Lu Y (2022) PPVED: a machine learning tool for predicting the effect of single amino acid substitution on protein function in plants. Plant Biotechnol J 20:1417–1431. https://doi.org/10.1111/pbi.13823
Hashimoto T, Mamishin S, Mouri A, Watabe A, Kondo M, Okada M, Wada T, Mise H, Oyagi T, Yotsuji T, Nodera Y, Nakazawa E (2012) Development of STEM for the HT7700 TEM and optimization of digital-image detectors arrangement. Microsc Microanal 18:1280–1281
Hussin SH, Wang H, Tang S, Zhi H, Tang C, Zhang W, Jia G, Diao X (2021) SiMADS34, an E-class MADS-box transcription factor, regulates inflorescence architecture and grain yield in Setaria italica. Plant Mol Biol 105:419–434
Jin F, Li S, Dang L, Chai W, Li P, Wang NN (2012) PL1 fusion gene: a novel visual selectable marker gene that confers tolerance to multiple abiotic stresses in transgenic tomato. Transgenic Res 21:1057–1070
Jung K, Hur J, Ryu C, Choi Y, Chung Y, Miyao A, Hirochika H, An G (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 44:463–472
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M (2007) Rice non-yellow coloring1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19:1362–1375
Lalitha S (2000) Primer premier 5. Biotech Softw Internet Rep 1:270–272
Li P, Brutnell TP (2011) Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses. J Exp Bot 62:3031–3037
Li W, Tang S, Zhang S, Shan J, Tang C, Chen Q, Jia G, Han Y, Zhi H, Diao X (2016) Gene mapping and functional analysis of the novel leaf color gene SiYGL1 in foxtail millet [Setaria italica (L.) P. Beauv]. Physiol Plant 157:24–37
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Lin H, Ashikari M, Yamanouchi U, Sasaki T, Yano M (2002) Identification and characterization of a quantitative trait locus, Hd9, controlling heading date in rice. Breed Sci 52:35–41
Ma X, Sun X, Li C, Huan R, Sun C, Wang Y, Xiao F, Wang Q, Chen P, Ma F (2017) Map-based cloning and characterization of the novel yellow-green leaf gene ys83 in rice (Oryza sativa). Plant Physiol Biochem 111:1–9
Muthamilarasan M, Prasad M (2015) Theor Appl Genet 128:1–14
Muthamilarasan M, Prasad M (2021) Small millets for enduring food security amidst pandemics. Trends Plant Sci 26(1):33–40. https://doi.org/10.1016/j.tplants.2020.08.008
Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the minolta SPAD-502 leaf chlorophyll meter. Photosynth Res 46:467–472
Masuda T (2008) Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynth Res 96:121–143
Nakanishi H, Nozue H, Suzuki K, Kaneko Y, Taguchi G, Hayashida N (2005) Characterization of the Arabidopsis thaliana mutant pcb2 which accumulates divinyl chlorophylls. Plant Cell Physiol 46:467–473
Papenbrock J, Gräfe S, Kruse E, Hänel F, Grimm B (1997) Mg-chelatase of tobacco: identification of a Chl D cDNA sequence encoding a third subunit, analysis of the interaction of the three subunits with the yeast two-hybrid system, and reconstitution of the enzyme activity by co-expression of recombinant CHL D, CHL H and CHL I. Plant J 12:981–990
Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155:1545–1551
Ren J, Liu Z, Niu R, Feng H, Debener T (2015) Mapping of Re, a gene conferring the red leaf trait in ornamental kale (Brassica oleracea L. var.acephala). Plant Breed 134:494–500
Sawers R, Viney J, Farmer P, Bussey R, Olsefski G, Anufrikova K, Hunter C, Brutnell TP (2006) The maize Oil yellow1 (Oy1) gene encodes the I subunit of magnesium chelatase. Plant Mol Biol 60:95–106
Soldatova O, Apchelimov A, Radukina N, Ezhova T, Shestakov S, Ziemann V, Hedtke B, Grimm B (2005) An Arabidopsis mutant that is resistant to the protoporphyrinogen oxidase inhibitor acifluorfen shows regulatory changes in tetrapyrrole biosynthesis. Mol Genet Genomics 273:311–318
Tang C, Tang S, Zhang S, Luo M, Jia G, Zhi H, Diao X (2018) SiSTL1, encoding a large subunit of ribonucleotide reductase, is crucial for plant growth, chloroplast biogenesis, and cell cycle progression in Setaria italica. J Exp Bot 70:1167–1182
Terry M, Kendrick R (1999) Feedback inhibition of chlorophyll synthesis in the phytochrome chromophore-deficient aurea and yellow-green-2 mutants of tomato. Plant Physiol 119:143–152
Walker CJ, Weinstein JD (1994) The magnesium-insertion step of chlorophyll biosynthesis is a two-stage reaction. Biochem J 299:277–284
Walker JC, Willows DR (1997) Mechanism and regulation of Mg-chelatase. Biochem J 327:321–333
Wan C, Li C, Ma X, Wang Y, Sun C, Huang R, Zhong P, Gao Z, Chen D, Xu Z (2015) GRY79 encoding a putative metallo-β-lactamase-trihelix chimera is involved in chloroplast development at early seedling stage of rice. Plant Cell Rep 34:1353–1363
Wilson-Sánchez D, Rubio-Díaz S, Muñoz-Viana R, Pérez-Pérez JM, Jover-Gil S, Ponce MR, Micol JL (2014) Leaf phenomics: a systematic reverse genetic screen for Arabidopsis leaf mutants. Plant J 79:878–891
Wu Z, Zhang X, He B, Diao L, Sheng S, Wang J, Guo X, Su N, Wang L, Jiang L (2007) A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiol 145:29–40
Yuan XY, Zhang LG, Huang L, Qi X, Wen YY, Dong SQ, Song XE, Wang HF, Guo PY (2017) Photosynthetic and physiological responses of foxtail millet (Setaria italica L.) to low-light stress during grain-filling stage. Photosynthetica 55:491–500
Zhang H, Li J, Yoo J-H, Yoo S-C, Cho S-H, Koh H-J, Seo HS, Paek N-C (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 Mol Biol 62:325–337
Zhang H, Liu L, Cai M, Zhu S, Zhao J, Zheng T, Xu X, Zeng Z, Niu J, Jiang L (2015) A point mutation of magnesium chelatase OsCHLI gene dampens the interaction between CHLI and CHLD subunits in rice. Plant Mol Biol Report 33:1975–1987
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 213:1–11
Zhang S, Tang S, Tang C, Luo M, Jia G, Zhi H, Diao X (2018a) SiSTL2 is required for cell cycle, leaf organ development, chloroplast biogenesis, and has effects on C4 photosynthesis in Setaria italica (L.) P. Beauv Front Plant Sci 9:1103. https://doi.org/10.3389/fpls.2018.01103
Zhang S, Zhi H, Li W, Shan J, Tang C, Jia G, Tang S, Diao X (2018b) SiYGL2 Is involved in the regulation of leaf senescence and photosystem II efficiency in Setaria italica (L.) P. Beauv Front Plant Sci 9:1308. https://doi.org/10.3389/fpls.2018.01308
Acknowledgements
This work was supported by grants from National Key Research and Development Program of China (2021YFF1000103), National Key R&D Program of China (nos. 2019YFD1000700/2019YFD1000701, and 2018YFD1000700), and China agricultural research system (CARS-06-13.5).
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XMD and HZ designed the experiment, developed the F2 population and revised the manuscript. HKL QH and HZ did data analysis and drafted the manuscript. ST and GQJ helped in the data analysis and discussion. HLW and QM helped to collect phenotypes. QH, XMD, ST and JHC revised the manuscript. All authors have read and approved the final manuscript.
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122_2023_4309_MOESM1_ESM.pdf
Supplementary file 1 Fig. S1 Photosynthetic indicators of 125A and S410 at the heading stage. Each condition includes measurements for three plants. Significant differences were determined using Student’s t test (ns: no significance)
122_2023_4309_MOESM2_ESM.pdf
Supplementary file 2 Fig. S2 Phylogenetic analysis of ortholog genes of SiCHLI in diverse plant species and their amino acid substitutions in foxtail millet. The species are as follows: B. sylvaticum, Brachypodium sylvaticum; T.aestivum, Triticum aestivum; A.thaliana, Arabidopsis thaliana; O.sativa, Oryza sativa; P.vaginatum, Paspalum vaginatum; Z.mays, Zea mays; S.bicolor, Sorghum bicolor; SiCHLI, Setaria italica; S.viridis, Setaria viridis
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Liang, H., He, Q., Zhang, H. et al. Identification and haplotype analysis of SiCHLI: a gene for yellow–green seedling as morphological marker to accelerate foxtail millet (Setaria italica) hybrid breeding. Theor Appl Genet 136, 24 (2023). https://doi.org/10.1007/s00122-023-04309-x
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DOI: https://doi.org/10.1007/s00122-023-04309-x