Abstract
Key message
A mutation of CsARC6 not only causes white fruit color in cucumber, but also affects plant growth and fruit quality.
Abstract
Fruit color of cucumber is a very important agronomic trait, but most of the genes affecting cucumber white fruit color are still unknow, and no further studies were reported on the effect of cucumber fruit quality caused by white fruit color genes. Here, we obtained a white fruit mutant em41 in cucumber by EMS mutagenesis. The mutant gene was mapped to a 548 kb region of chromosome 2. Through mutation site analysis, it was found to be a null allele of CsARC6 (CsaV3_2G029290). The Csarc6 mutant has a typical phenotype of arc6 mutant that mesophyll cells contained only one or two giant chloroplasts. ARC6 protein was not detected in em41, and the level of FtsZ1 and FtsZ2 was also reduced. In addition, FtsZ2 could not form FtsZ ring-like structures in em41. Although these are typical arc6 mutant phenotypes, some special phenotypes occur in Csarc6 mutant, such as dwarfness with shortened internodes, enlarged fruit epidermal cells, decreased carotenoid contents, smaller fruits, and increased fruit nutrient contents. This study discovered a new gene, CsARC6, which not only controls the white fruit color, but also affects plant growth and fruit quality in cucumber.
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All data generated or analyzed during this study are included in this published article and its supplementary information files.
Change history
09 June 2023
A Correction to this paper has been published: https://doi.org/10.1007/s00122-023-04382-2
Abbreviations
- ARC6:
-
Accumulation and replication of chloroplasts 6
- FtsZ:
-
Filamenting temperature-sensitive mutant Z
- Fv′/Fm′:
-
PSII effective photochemical efficiencies under light
- Fq′/Fv′:
-
Photochemical quenching coefficient qP
- Fq′/Fm′:
-
Light quantum efficiency
- NPQ:
-
Steady state nonphotochemical quenching
- PARC6:
-
Paralog of ARC6
- WT:
-
Wild type
References
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113. https://doi.org/10.1146/annurev.arplant.59.032607.092759
Brand A, Borovsky Y, Hill T, Rahman KAA, Bellalou A, Deynze AV, Paran I (2014) CaGLK2 regulates natural variation of chlorophyll content and fruit color in pepper fruit. Theor Appl Genet 127:2139–2148. https://doi.org/10.1007/s00122-014-2367-y
Chang J, Zhang F, Qin H, Liu P, Wang J, Wu S (2021) Mutation of SlARC6 leads to tissue-specific defects in chloroplast development in tomato. Hortic Res 8:127. https://doi.org/10.1038/s41438-021-00567-2
Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of the β-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and abscisic acid synthesis in rice. Plant Physiol 154:1304–1318. https://doi.org/10.1104/pp.110.163741
Fujiwara MT, Yasuzawa M, Kojo KH, Niwa Y, Abe T, Yoshida S, Nakano T, Itoh RD (2018) The Arabidopsis arc5 and arc6 mutations differentially affect plastid morphology in pavement and guard cells in the leaf epidermis. PLoS ONE 13:e0192380. https://doi.org/10.1371/journal.pone.0192380
Gao YF, Liu H, An CJ, Shi YH, Liu X, Yuan WQ, Zhang B, Yang J, Yu CX, Gao HB (2013) Arabidopsis FRS4/CPD25 and FHY3/CPD45 work cooperatively to promote the expression of the chloroplast division gene ARC5 and chloroplast division. Plant J 75:795–807. https://doi.org/10.1111/tpj.12240
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA Gen Subj 990:87–92. https://doi.org/10.1146/annurev.arplant.59.032607.092759
Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460–2470. https://doi.org/10.1105/tpc.108.061440
Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY, Osteryoung KW (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59:700–711. https://doi.org/10.1111/j.1365-313X.2009.03905.x
Hao N, Du YL, Li HY, Wang C, Wang C, Gong SY, Zhou SM, Wu T (2018) CsMYB36 is involved in the formation of yellow green peel in cucumber (Cucumis Sativus L.). Theor Appl Genet 131:1659–1669. https://doi.org/10.1007/s00122-018-3105-7
Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynth Res 34:375–385. https://doi.org/10.1007/BF00029812
Hughes DE (1983) Titrimetric determination of ascorbic acid with 2,6-dichlorophenol indophenol in commercial liquid diets. J Pharm Sci US 72:126–129. https://doi.org/10.1002/jps.2600720208
Jeong WJ, Park YI, Suh KH, Raven JA, Liu Y (2002) A large population of small chloroplasts in tobacco leaf cells allows more effective chloroplast movement than a few enlarged chloroplasts. Plant Physiol 129:112–121. https://doi.org/10.1104/pp.000588
Jiao JQ, Liu HQ, Liu J, Cui MM, Xu J, Meng HW, Li YH, Chen SX, Cheng ZH (2017) Identification and functional characterization of APRR2 controlling green immature fruit color in cucumber (Cucumis Sativus L.). Plant Growth Regul 83:233–243. https://doi.org/10.1007/s10725-017-0304-1
Kishor DS, Alavilli H, Lee S-C, Kim J-G, Song K (2021) Development of SNP markers for white immature fruit skin color in cucumber (Cucumis Sativus L.) using QTL-seq and marker analyses. Plants 10:2314. https://doi.org/10.3390/plants10112341
Kohchi T, Mukougawa K, Frankenberg N, Masuda M, Yokota N, Yokota A, Lagarias JC (2001) The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 13:425–436. https://doi.org/10.1105/tpc.13.2.425
Koksharova OA, Wolk CP (2002) A novel gene that bears a DnaJ motif influences cyanobacterial cell division. J Bacteriol 184:5524–5528. https://doi.org/10.1128/JB.184.19.5524-5528.2002
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) Mega X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Li YQ, Sun QQ, Feng Y, Liu XM, Gao HB (2016) An improved immunofluorescence staining method for chloroplast proteins. Plant Cell Rep 35:2285–2293. https://doi.org/10.1007/s00299-016-2034-7
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Liu HQ, Meng HW, Pan YP, Liang XJ, Jiao JQ, Li YH, Chen SX, Cheng ZH (2015) Fine genetic mapping of the white immature fruit color gene w to a 33.0-kb region in cucumber (Cucumis Sativus L.). Theor Appl Genet 128:2375–2385. https://doi.org/10.1007/s00122-015-2592-z
Liu HQ, Jiao JQ, Liang XJ, Liu J, Meng HW, Chen SX, Li YH, Cheng ZH (2016) Map-based cloning, identification and characterization of the w gene controlling white immature fruit color in cucumber (Cucumis Sativus L.). Theor Appl Genet 129:1247–1256. https://doi.org/10.1007/s00122-016-2700-8
Liu XM, An JJ, Wang LL et al (2022) A novel amphiphilic motif at the C-terminus of Ftsz1 facilitates chloroplast division. Plant Cell 34:419–432. https://doi.org/10.1093/plcell/koab272
Lun YY, Wang X, Zhang CZ, Yang L, Gao DL, Chen HM, Huang SW (2016) A CsYcf54 variant conferring light green coloration in cucumber. Euphytica 208:509–517. https://doi.org/10.1007/s10681-015-1592-z
Maple J, Aldridge C, Møller SG (2005) Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J 43:811–823. https://doi.org/10.1111/j.1365-313X.2005.02493.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
Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134. https://doi.org/10.1105/tpc.10.7.1121
Osteryoung KW, Pyke KA (2014) Division and dynamic morphology of plastids. Annu Rev Plant Biol 65:443–472. https://doi.org/10.1146/annurev-arplant-050213-035748
Pyke KA, Forth D (2006) The suffulta mutation in tomato reveals a novel method of plastid replication during fruit ripening. J Exp Bot 57:1971–1979. https://doi.org/10.1093/jxb/erj144
Pyke KA, Leech RM (1991) Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) heynh. Plant Physiol 96:1193–1195. https://doi.org/10.1104/pp.96.4.1193
Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104:201–207. https://doi.org/10.1104/pp.104.1.201
Pyke KA, Rutherford SM, Robertson EJ, Leech RM (1994) arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol 106:1169–1177. https://doi.org/10.1104/pp.106.3.1169
Qi WZ, Zhao L (2013) Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microb 53:355–364. https://doi.org/10.1002/jobm.201200031
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. Mol Breeding 33:1–14. https://doi.org/10.1007/s11032-013-9917-x
Shan N, Gan ZY, Nie J, Liu H, Wang ZY, Sui XL (2020) Comprehensive characterization of fruit volatiles and nutritional quality of three cucumber (Cucumis Sativus L.) genotypes from different geographic groups after bagging treatment. Foods 9:294. https://doi.org/10.3390/foods9030294
Sui XL, Shan N, Hu LP, Zhang CK, Yu CQ, Ren HZ, Robert T, Zhang ZX (2017) The complex character of photosynthesis in cucumber fruit. J Exp Bot 7:1625–1637. https://doi.org/10.1093/jxb/erx034
Sun WK, Ma N, Huang HY, Wei JW, Ma S, Liu H, Zhang S, Zhang ZX, Sui XL, Li X (2021) Photosynthetic contribution and characteristics of cucumber stem and petiole. BMC Plant Biol 21:454. https://doi.org/10.1186/s12870-021-03233-w
Takagi H, Abe A, Yoshida K et al (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183. https://doi.org/10.1111/tpj.12105
Tang HY, Dong X, Wang JK, Xia JH, Xiu F, Zhang Y, Yao X, Xu YJ, Wang ZJ (2018) Fine mapping and candidate gene prediction for white immature fruit skin in cucumber (Cucumis Sativus L.). Int J Mol Sci 19:1493. https://doi.org/10.3390/ijms19051493
Vitha S, Froehlich JE, Koksharova O, Pyke KA, Erp HV, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933. https://doi.org/10.1105/tpc.013292
Wang WH, Li JY, Sun QQ et al (2017) Structural insights into the coordination of plastid division by the ARC6–PDV2 complex. Nat Plants 3:17011. https://doi.org/10.1038/nplants.2017.11
Xie JH, Wehner TC (2001) Gene list 2001 for cucumber. Cucurbit Genet Coop Rep 24:110–136
Zhang LY, Peng YB, Pelleschi-Travie RS, Fan Y, Lu YF, Lu YM, Gao XP, Shen YY, Delrot S, Zhang DP (2004) Evidence for apoplasmic phloem unloading in developing apple fruit. Plant Physiol 135:574–586. https://doi.org/10.1104/pp.103.036632
Acknowledgements
We thank Professor Zhenxian Zhang (China Agricultural University of Vegetable Science) and Jiawang Li (Tianjin Kerenl Cucumber Research Institute) for providing the initial idea of this paper, and the cucumber breeding materials.
Funding
This work was supported by the National Key Research and Development Program of China (2019YFD1000300); the National Natural Science Foundation of China (grant nos. 32070696 and 31801850); Tianjin Natural Science Foundation Project (20JCYBJC00720); the Beijing Innovation Consortium of Agriculture Research System (BAIC01-2022); the Key Research and Development Program of Ningxia (2021BBF02005); the 111 Project (B17043); and the Construction of Beijing Science and Technology Innovation and Service Capacity in Top Subjects (CEFF-PXM2019_014207_000032).
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XL and HG conceived and designed the experiments; WS, XL and HH performed the experiments; XL, HG, WS and XL wrote the manuscript; JW, FZ, YH, QS and WM assisted in performing the experiments; YT, YL and LG assisted in the selection and breeding of mutant materials. All authors read and approved the final manuscript.
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Communicated by Hong-Qing Ling.
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Sun, W., Li, X., Huang, H. et al. Mutation of CsARC6 affects fruit color and increases fruit nutrition in cucumber. Theor Appl Genet 136, 111 (2023). https://doi.org/10.1007/s00122-023-04337-7
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DOI: https://doi.org/10.1007/s00122-023-04337-7