Abstract
Key message
A SNP mutation in CmYGP gene encoding Golden2-like transcription factor is responsible for melon yellow-green plant trait.
Abstract
Chlorophylls are essential and beneficial substances for both plant and human health. Identifying the regulatory network of chlorophyll is necessary to improve the nutritional quality of fruits. At least six etiolation genes have been identified in different melon varieties, but none of them have been cloned, and the molecular mechanisms underlying chlorophyll synthesis and chloroplast development in melon remain unclear. Here, the NSL73046, a yellow-green plant (Cmygp) mutant, enabled the map-based cloning of the first etiolation gene in melon. CmYGP encodes a Golden2-like transcription factor. Spatiotemporal expression analyses confirmed the high CmYGP expression in all green tissues, particularly in young leaves and fruit peels. Virus-induced gene silencing and the development of near-isogenic line by marker-assisted selection further confirmed that downregulation of CmYGP can reduce chloroplast number and chlorophyll content, thereby resulting in yellow-green leaves and fruits in melon, and overexpression of CmYGP in tomatoes also led to dark-green leaves and fruits. RNA-seq analysis revealed that CmYGP greatly affected the expression of key genes associated with chloroplast development. Taken together, these findings demonstrated that CmYGP regulate chlorophyll synthesis and chloroplast development thus affect fruit development in melon. This study also offers a new strategy to enhance fruit quality in melon.
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Data availability
The raw data of RNA-seq are accessible at NCBI under the BioProject PRJNA868299. The plant material and datasets employed in this study are available from the corresponding author on reasonable request. The genomic resequence datasets of two melon materials have been deposited into the NCBI sequence read archive (SRA) SRP119828 under accessions SRS2585930 and SRS2585931.
References
Arnon DI (1949) Copper enzymes in isolated chloroplasts Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1. https://doi.org/10.1104/pp.24.1.1
Cackett L, Luginbuehl LH, Schreier TB, Lopez-Juez E, Hibberd JM (2022) Chloroplast development in green plant tissues: the interplay between light, hormone, and transcriptional regulation. New Phytol 233(5):2000–2016. https://doi.org/10.1111/nph.17839
Chang WL, Soll J, Bölter B (2012) The gateway to chloroplast: re-defining the function of chloroplast receptor proteins. Biol Chem 393:1263–1277. https://doi.org/10.1515/hsz-2012-0235
Chen M, Ji M, Wen B, Liu L, Li S, Chen X, Gao D, Li L (2016a) GOLDEN 2-LIKE transcription factors of plants. Front Plant Sci 7:1509. https://doi.org/10.3389/fpls.2016.01509
Chen C, Yin S, Liu X, Liu B, Yang S, Xue S, Cai Y, Black K, Liu H, Dong M (2016b) The WD-repeat protein CsTTG1 regulates fruit wart formation through interaction with the homeodomain-leucine zipper I protein Mict. Plant Physiol 171:1156–1168. https://doi.org/10.1104/pp.16.00112
Chen M, Liu X, Jiang S, Wen B, Yang C, Xiao W, Fu X, Li D, Chen X, Gao D (2018) Transcriptomic and functional analyses reveal that PpGLK1 regulates chloroplast development in peach (Prunus persica). Front Plant Sci 9:34. https://doi.org/10.3389/fpls.2018.00034
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Cocaliadis MF, Fernández-Muñoz R, Pons C, Orzaez D, Granell A (2014) Increasing tomato fruit quality by enhancing fruit chloroplast function. A double-edged sword? J Exp Bot 65:4589–4598. https://doi.org/10.1093/jxb/eru165
DeLuca DS, Levin JZ, Sivachenko A, Fennell T, Nazaire M-D, Williams C, Reich M, Winckler W, Getz G (2012) RNA-SeQC: RNA-seq metrics for quality control and process optimization. Bioinformatics 28:1530–1532. https://doi.org/10.1093/bioinformatics/bts196
Ding X, Jimenez-Gongora T, Krenz B, Lozano-Duran R (2019) Chloroplast clustering around the nucleus is a general response to pathogen perception in Nicotiana benthamiana. Mol Plant Pathol 20:1298–1306. https://doi.org/10.1111/mpp.12840
Dyutin KE (1979) Inheritance of yellow-green coloration of the young leaves in melon (in Russian). Tsitologia i Genetika 13:407–408
Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31:713–727. https://doi.org/10.1046/j.1365-313X.2002.01390.x
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. Theor Appl Genet 129(10):1961–1973. https://doi.org/10.1007/s00122-016-2752-9
Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM, Hénaff E, Câmara F, Cozzuto L, Lowy E (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci 109:11872–11877. https://doi.org/10.1073/pnas.1205415109
Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994. https://doi.org/10.1007/BF00014672
Hoffman JC, Nugent PE (1973) Inheritance of a virescent mutant in muskmelon. J Hered 64:311–312. https://doi.org/10.1093/oxfordjournals.jhered.a108427
Huang Y-S, Li H-m (2009) Arabidopsis CHLI2 can substitute for CHLI1. Plant Physiol 150:636–645. https://doi.org/10.1104/pp.109.135368
Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Report 5:387–405. https://doi.org/10.1007/BF02667740
Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Ann Rev Genet 45:41–59. https://doi.org/10.1146/annurev-genet-110410-132507
Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Keränen M, Aro E-M, Fukaki H, Ohta H, Sugimoto K (2012) Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell 24:1081–1095. https://doi.org/10.1105/tpc.111.092254
Kobayashi K, Narise T, Sonoike K, Hashimoto H, Sato N, Kondo M, Nishimura M, Sato M, Toyooka K, Sugimoto K (2013) Role of galactolipid biosynthesis in coordinated development of photosynthetic complexes and thylakoid membranes during chloroplast biogenesis in Arabidopsis. Plant J 73:250–261. https://doi.org/10.1111/tpj.12028
Kobayashi K, Fujii S, Sasaki D, Baba S, Ohta H, Masuda T, Wada H (2014) Transcriptional regulation of thylakoid galactolipid biosynthesis coordinated with chlorophyll biosynthesis during the development of chloroplasts in Arabidopsis. Front Plant Sci 5:272. https://doi.org/10.3389/fpls.2014.00272
Li X, Huang S, Liu Z, Hou L, Feng H (2019) Mutation in EMB1923 gene promoter is associated with chlorophyll deficiency in Chinese cabbage (Brassica campestris ssp. pekinensis). Physiol Plant 166:909–920. https://doi.org/10.1111/ppl.12979
Lichtenthaler HK (1987) [34] Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Liu L, Jia C, Zhang M, Chen D, Chen S, Guo R, Guo D, Wang Q (2014) Ectopic expression of a BZR1-1D transcription factor in brassinosteroid signalling enhances carotenoid accumulation and fruit quality attributes in tomato. Plant Biotechnol J 12:105–115. https://doi.org/10.1111/pbi.12121
Liu M, Liang Z, Aranda MA, Hong N, Liu L, Kang B, Gu Q (2020) A cucumber green mottle mosaic virus vector for virus-induced gene silencing in cucurbit plants. Plant Methods 16:1–13. https://doi.org/10.1186/s13007-020-0560-3
Liu G, Yu H, Yuan L, Li C, Ye J, Chen W, Wang Y, Ge P, Zhang J, Ye Z (2021) SlRCM1, which encodes tomato Lutescent1, is required for chlorophyll synthesis and chloroplast development in fruits. Horticult Res 8:1–14. https://doi.org/10.1038/s41438-021-00563-6
Miao H, Zhang S, Wang M, Wang Y, Weng Y, Gu X (2016) Fine Mapping of Virescent Leaf Gene v–1 in Cucumber (Cucumis sativus L.). Int J Mol Sci 17(10):1602. https://doi.org/10.3390/ijms17101602
Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392. https://doi.org/10.1046/j.1365-313X.1998.00124.x
Nguyen CV, Vrebalov JT, Gapper NE, Zheng Y, Zhong S, Fei Z, Giovannoni JJ (2014) Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening. Plant Cell 26:585–601. https://doi.org/10.1105/tpc.113.118794
Nugent PE, Hoffman JC (1974) Inheritance of the halo cotyledon mutant in muskmelon. J Hered 65:315–316. https://doi.org/10.1093/oxfordjournals.jhered.a108537
Ouyang B, Chen YH, Li HX, Qian CJ, Huang SL, Ye ZB (2005) Transformation of tomatoes with osmotin and chitinase genes and their resistance to Fusarium wilt. J Horticult Sci Biotechnol 80:517–522. https://doi.org/10.1080/14620316.2005.11511971
Pitrat M (1991) Linkage groups in Cucumis melo L. J Hered 82:406–411. https://doi.org/10.1093/oxfordjournals.jhered.a111112
Powell AL, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, Bennett AB (2012) Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336(6089):1711–1715. https://doi.org/10.1126/science.1222218
Rissler HM, Collakova E, DellaPenna D, Whelan J, Pogson BJ (2002) Chlorophyll biosynthesis. Expression of a second chl I gene of magnesium chelatase in Arabidopsis supports only limited chlorophyll synthesis. Plant Physiol 128:770–779. https://doi.org/10.1104/pp.010625
Sagar M, Chervin C, Mila I, Hao Y, Roustan J-P, Benichou M, Gibon Y, Biais B, Maury P, Latché A (2013) SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol 161:1362–1374. https://doi.org/10.1104/pp.113.213843
Shi Y, Pang X, Liu W, Wang R, Su D, Gao Y, Wu M, Deng W, Liu Y, Li Z (2021) SlZHD17 is involved in the control of chlorophyll and carotenoid metabolism in tomato fruit. Horticult Res 8:1–16. https://doi.org/10.1038/s41438-021-00696-8
Song M, Wei Q, Wang J, Fu W, Qin X, Lu X, Cheng F, Yang K, Zhang L, Yu X (2018) Fine mapping of CsVYL, conferring virescent leaf through the regulation of chloroplast development in cucumber. Front Plant Sci 9:432. https://doi.org/10.3389/fpls.2018.00432
Taketa S, Hattori M, Takami T, Himi E, Sakamoto W (2021) Mutations in a Golden2-like gene cause reduced seed weight in barley albino lemma 1 mutants. Plant Cell Physiol 62(3):447–457. https://doi.org/10.1093/pcp/pcab001
Terry MJ, Kendrick RE (1999) Feedback inhibition of chlorophyll synthesis in the phytochrome chromophore-deficient aurea and yellow-green-2 mutants of tomato. Plant Physiol 119(1):143–152. https://doi.org/10.1104/pp.119.1.143
Wang P, Fouracre J, Kelly S, Karki S, Gowik U, Aubry S, Shaw MK, Westhoff P, Slamet-Loedin IH, Quick WP (2013) Evolution of GOLDEN2-LIKE gene function in C 3 and C 4 plants. Planta 237:481–495. https://doi.org/10.1007/s00425-012-1754-3
Whitaker TW (1952) Genetic and chlorophyll studies of a yellow-green mutant in muskmelon. Plant Physiol 27:263. https://doi.org/10.1104/pp.27.2.263
Yang Y, Chen X, Xu B, Li Y, Ma Y, Wang G (2015) Phenotype and transcriptome analysis reveals chloroplast development and pigment biosynthesis together influenced the leaf color formation in mutants of Anthurium andraeanum ‘Sonate.’ Front Plant Sci 6:139. https://doi.org/10.3389/fpls.2015.00139
Yang S, Cai Y, Liu X, Dong M, Zhang Y, Chen S, Zhang W, Li Y, Tang M, Zhai X (2018) A CsMYB6-CsTRY module regulates fruit trichome initiation in cucumber. J Exp Bot 69:1887–1902. https://doi.org/10.1093/jxb/ery047
Yang S, Wen C, Liu B, Cai Y, Xue S, Bartholomew ES, Dong M, Jian C, Xu S, Wang T (2019) A CsTu-TS 1 regulatory module promotes fruit tubercule formation in cucumber. Plant Biotechnol J 17:289–301. https://doi.org/10.1111/pbi.12977
Yang S, Zhang K, Zhu H, Zhang X, Yan W, Xu N, Liu D, Hu J, Wu Y, Weng Y (2020) Melon short internode (CmSi) encodes an ERECTA-like receptor kinase regulating stem elongation through auxin signaling. Horticult Res 7:1–14. https://doi.org/10.1038/s41438-020-00426-6
Zhang Y, Zhang X, Liu B, Wang W, Liu X, Chen C, Liu X, Yang S, Ren H (2014) A GAMYB homologue CsGAMYB1 regulates sex expression of cucumber via an ethylene-independent pathway. J Exp Bot 65:3201–3213. https://doi.org/10.1093/jxb/eru176
Zhao G, Lian Q, Zhang Z, Fu Q, He Y, Ma S, Ruggieri V, Monforte AJ, Wang P, Julca I (2019) A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat Genet 51:1607–1615. https://doi.org/10.1038/s41588-019-0522-8
Zhu H, Song P, Koo D-H, Guo L, Li Y, Sun S, Weng Y, Yang L (2016) Genome wide characterization of simple sequence repeats in watermelon genome and their application in comparative mapping and genetic diversity analysis. BMC Genomics 17:1–17. https://doi.org/10.1186/s12864-016-2870-4
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. J Exp Bot 68(15):4125–4135. https://doi.org/10.1093/jxb/erx240
Zhu H, Sun X, Zhang Q, Song P, Hu Q, Zhang X, Li X, Hu J, Pan J, Sun S, Weng Y, Yang L (2018) GLABROUS (CmGL) encodes a HD-ZIP IV transcription factor playing roles in multicellular trichome initiation in melon. Theor Appl Genet 131(3):569–579. https://doi.org/10.1007/s00122-017-3019-9
Zhu Y, Yuan G, Wang Y, An G, Li W, Liu J, Sun D (2022) Mapping and functional verification of leaf yellowing genes in watermelon during whole growth period. Front Plant Sci 19(13):1049114. https://doi.org/10.3389/fpls.2022.1049114
Zink F (1977) Linkage of virescent foliage and plant growth habit in muskmelon. J Am Soc Horticult Sci 102(5):613–615. https://doi.org/10.21273/JASHS.102.5.613
Acknowledgments
This study was supported by the National Natural Science Foundation of China (31872133, 32072600, 31902038, 31872101, 32072564), Natural Science Foundation of Henan Province (212300410048), the Zhongyuan Youth Talent Program (ZYQR201912161), Program for Science & Technology Innovation Talents of Henan Province (21HASTIT038, 23HASTIT034), the Key Scientific and Technological Project of Henan Province (212102110397), the Training plan for young backbone teachers in Universities of Henan Province (2020GGJS045).
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LY, SS, HZ design of the research. YZ and PS performed the gene mapping. SY, XW, WY, YG, KX, JH, and YW contributed to data analysis. LY and SY wrote the manuscript. All authors reviewed and approved this manuscript.
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Yang, S., Wang, X., Yan, W. et al. Melon yellow-green plant (Cmygp) encodes a Golden2-like transcription factor regulating chlorophyll synthesis and chloroplast development. Theor Appl Genet 136, 66 (2023). https://doi.org/10.1007/s00122-023-04343-9
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DOI: https://doi.org/10.1007/s00122-023-04343-9