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Journal of Integrative Agriculture  2017, Vol. 16 Issue (09): 1956-1967    DOI: 10.1016/S2095-3119(16)61618-0
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Effect of ploidy level on expression of lycopene biosynthesis genes and accumulation of phytohormones during watermelon (Citrullus lanatus) fruit development and ripening
DOU Jun-ling1, 2, YUAN Ping-li1, ZHAO Sheng-jie1, HE Nan1, ZHU Hong-ju1, 2, GAO Lei1, JI Wan-li1, LU Xu-qiang1, LIU Wen-ge1
1 Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou 450009, P.R.China
2 College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, P.R.China
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Abstract  The difference between lycopene and phytohormone levels among diploid, triploid and tetraploid plants of two watermelon cultivars during fruit growth and ripening was studied.  The expression pattern of five genes (phytoene synthase (PSY1), phytoene desaturase (PDS), ζ-carotene desaturase (ZDS), carotenoid isomerase (CRTISO), and lycopene β-cyclase (LCYB)) was analyzed in details.  In red-fleshed cultivar Mimei, lycopene content increased rapidly from 25 to 35 days after pollination (DAP), and then decreased at 40 DAP.  Triploid and tetraploid fruit had higher levels of lycopene than diploid.  Moreover, triploid tended to contain more lycopene than tetraploid during fruit growth and ripening stages.  However, little amount of lycopene (0–2 mg kg–1 fresh weight (FW)) in yellow-fleshed cultivar Huangmei was found during all fruit development stages.  In Mimei, transcript level of PSY1 was generally higher than the other four genes, and LCYB gene expression was the lowest among all five genes being tested.  PSY1, CRTISO and LCYB genes showed higher transcript levels in polyploid than in diploid fruit.  By contrast, in Huangmei, transcript level of LCYB was not the lowest, but only lower than that of PSY1PSY1, CRTISO and LCYB genes showed higher expression levels in diploid than in polyploid fruit.  In Mimei, the negative correlation between gibberellane (GA) content and lycopene accumulation was determined in all three different ploidy fruits, while a positive correlation was observed between abscisic acid (ABA) content and lycopene accumulation only in diploid watermelon.  These results indicated that different lycopene contents in different ploidy watermelons is regulated by the differential transcription expression of the lycopene metabolic genes and phytohormones. 
Keywords:  watermelon        lycopene       gene expression       ploid       flesh color        phytohormone  
Received: 01 November 2016   Accepted:
Fund: 

This work was supported by the National Natural Science Foundation of China (31171979 and 31471893), the Agricultural Science and Technology Innovation Program, China (ASTIP) (CAAS-ASTIP-2017-ZFRI), the earmarked fund for the China Agriculture Research System (CARS-26-03), and the Central Public-interest Scientific Institution Basal Research Fund, China (1610192016301 and 1616032017209).

Corresponding Authors:  Correspondence LU Xu-qiang, E-mail: luxuqiang123@163.com; LIU Wen-ge, Tel: +86-371-65330936, E-mail: lwgwm@163.com   
About author:  DOU Jun-ling, E-mail: junlingdou@163.com

Cite this article: 

DOU Jun-ling, YUAN Ping-li, ZHAO Sheng-jie, HE Nan, ZHU Hong-ju, GAO Lei, JI Wan-li, LU Xuqiang, LIU Wen-ge. 2017. Effect of ploidy level on expression of lycopene biosynthesis genes and accumulation of phytohormones during watermelon (Citrullus lanatus) fruit development and ripening. Journal of Integrative Agriculture, 16(09): 1956-1967.

Alquézar B, Zacarías L, Rodrigo M J. 2009. Molecular and functional characterization of a novel chromoplast-specific lycopene β-cyclase from Citrus and its relation to lycopene accumulation. Journal of Experimental Botany, 60, 1783–1797.

Auldridge M E, McCarty D R, Klee H J. 2006. Plant carotenoid cleavage oxygenases and their apocarotenoid products. Current Opinion Plant Biology, 9, 315–321.

Bang H, Davis A R, Kim S, Leskovar D I, King S R. 2010. Flesh color inheritance and gene interactions among canary yellow, pale yellow, and red watermelon. Journal of the American Society for Horticultural Science, 135, 362–368.

Bang H, Kim S, Leskovar D, King S. 2007. Development of a codominant CAPS marker for allelic selection between canary yellow and red watermelon based on SNP in lycopene β-cyclase (LCYB) gene. Molecular Breeding, 20, 63–72.

Bang H, Kim S, Leskovar D, King S. 2004. Differential expression of carotenoid biosynthesis genes among different colored flesh in watermelons (Citrullus lanatus (Thunb)). HortScience, 39, 869–870.

Bang H J. 2007. Environmental and genetic strategies to improve carotenoids and quality in watermelon. Ph D thesis, Texas A&M University, USA.

Bramley P M. 2002. Regulation of carotenoid formation during tomato fruit ripening and development. Journal of Experimental Botany, 53, 2107–2113.

Buggs R J, Elliott N M, Zhang L, Koh J, Viccini L F, Soltis D E. 2010. Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. New Phytologist, 186, 175–183.

Clotault J, Peltier D, Berruyer R, Thomas M, Briard M, Geoffriau E. 2008. Expression of carotenoid biosynthesis genes during carrot root development. Journal of Experimental Botany, 59, 3563–3573.

Cunningham F X. 2002. Regulation of carotenoid synthesis and accumulation in plants. Pure and Applied Chemistry, 74, 1409–1417.

Dou J L, Liu W G, Zhao S J, Lu Q, He N, Zhu H J. 2014. Expression of lycopene synthesis and metabolism genes during maturation of triploid seedless watermelon. Journal of Fruit Science, 31, 589–595. (in Chinese)

Dun E A, Brewer P B, Beveridge C A. 2009. Strigolactones: Discovery of the elusive shoot branching hormone. Trends in Plant Science, 14, 364–372.

Fraser P D, Bramley P M. 2004. The biosynthesis and nutritional uses of carotenoids. Progress in Lipid Research, 43, 228–265.

Fraser P D, Enfissi E M, Bramley P M. 2009. Genetic engineering of carotenoid formation in tomato fruit and the potential application of systems and synthetic biology approaches. Archives Biochemistry Biophysics, 483, 196–204.

Fraser P D, Romer S, Shipton C A, Mills P B, Kiano J W, Misawa N. 2002. Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proceedings of the National Academy of Sciences, 99, 1092–1097.

Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J. 2008. Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. The Plant Journal, 53, 717–730.

Goff S A, Klee H J. 2006. Plant volatile compounds: Sensory cues for health and nutritional value? Science, 311, 815–819.

Grassi S, Piro G, Lee J, Zheng Y, Fei Z, Dalessandro G. 2013. Comparative genomics reveals candidate carotenoid pathway regulators of ripening watermelon fruit. BMC Genomics, 14, 781.

Wang G Y, Xia R X. 2005. Changes in the contents of lycopene, beta-carotene, sugar and endogenous GA and ABA in flesh during the fruit development of ‘Cara Cara’ orange. Acta Horticulturae Sinica, 32, 482. (in Chinese)

Guo S, Liu J, Zheng Y, Huang M, Zhang H, Gong G. 2011. Characterization of transcriptome dynamics during watermelon fruit development: Sequencing, assembly, annotation and gene expression profiles. BMC Genomics, 12, 1.

Guo S, Sun H, Zhang H, Liu J, Ren Y, Gong G, Xu Y. 2015. Comparative transcriptome analysis of cultivated and wild watermelon during fruit development. PLOS ONE, 10, e0130267.

Howe J A, Tanumihardjo S A. 2006. Evaluation of analytical methods for carotenoid extraction from biofortified maize (Zea mays sp.). Journal of Agricultural and Food Chemistry, 54, 7992–7997.

Jeffery J, Davis A, King S. 2012. Understanding the carotenoid biosynthetic pathway: Observation of four color variants of developing watermelon fruit. Israel Journal of Plant Science, 60, 425–434.

Kang B, Zhao W, Hou Y, Tian P. 2010. Expression of carotenogenic genes during the development and ripening of watermelon fruit. Scientia Horticulturae, 124, 368–375.

Kato M, Ikoma Y, Matsumoto H, Sugiura M, Hyodo H, Yano M. 2004. Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiology, 134, 824–837.

Lee J M, Joung J G, McQuinn R, Chung M Y, Fei Z, Tieman D. 2012. Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. The Plant Journal, 70, 191–204.

Li J G, Guo S D. 2004. Extraction of total RNA and cloning of

      conservative fragments of MADS-box gene by RT-PCR in Upland cotton. Cotton Science, 16, 3–7.

Liu B H, Jiang Y M, Peng F T, Sui J, Zhao F X, Wang H Y. 2007. The dynamic changes of endogenous hormones in sweet cherry (Prunus avium L.) pulp. Acta Horticulturae Sinica, 34, 1535. (in Chinese)

Liu L, Wei J, Zhang M, Zhang L, Li C, Wang Q. 2012. Ethylene independent induction of lycopene biosynthesis in tomato fruits by jasmonates. Journal of Experimental Botany, 16, 5751-5761.

Liu W G, Yan Z H, Rao X L. 2005. Comparison of the leaf epidermal ultra-structure morphology of different ploidy watermelon. Journal of Fruit Science, 1, 31-34. (in Chinese)

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods, 25, 402–408.

Luan L, Kong F, He T, Liu G, Tu S. 2003. Genetic variation of tetraploid and diploid rice revealed by microsatellite marks. Chinese Journal of Applied and Environmental Biology, 10, 556–558.

Lü P, Li N, Liu H, Gu H, Zhao W. 2015. Changes in carotenoid profiles and in the expression pattern of the genes in carotenoid metabolisms during fruit development and ripening in four watermelon cultivars. Food Chemistry, 174, 52–59.

Maass D, Arango J, Wüst F, Beyer P, Welsch R. 2009. Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS One, 4, e6373.

O’Donnell P J, Schmelz E, Block A, Miersch O, Wasternack C, Jones J B. 2003. Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiology, 133, 1181–1189.

Pecker I, Gabbay R, Cunningham Jr F X, Hirschberg J. 1996. Cloning and characterization of the cDNA for lycopene β-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Molecular Biology, 30, 807–819.

Qin G, Gu H, Ma L, Peng Y, Deng X  W, Chen Z. 2007. Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in Arabidopsis by impairing chlorophyll, carotenoid, and gibberellin biosynthesis. Cell Research, 17, 471–482.

Rodrigo M J, Marcos J F, Zacarías L. 2004. Biochemical and molecular analysis of carotenoid biosynthesis in flavedo of orange (Citrus sinensis L.) during fruit development and maturation. Journal of Agricultural and Food Chemistry, 52, 6724–6731.

Rodriguez-Amaya D B. 2001. A Guide to Carotenoid Analysis in Foods. ILSI Press, Washington, D.C. p. 65.

Ronen G, Cohen M, Zamir D, Hirschberg J. 1999. Regulation of carotenoid biosynthesis during tomato fruit development: Expression of the gene for lycopene epsiloncyclase is down-regulated during ripening and is elevated in the mutantDelta. The Plant Journal, 17, 341–351.

Roulin A, Auer P L, Libault M, Schlueter J, Farmer A, May G. 2013. The fate of duplicated genes in a polyploid plant genome. The Plant Journal, 73, 143–153.

Schwartz S H, Tan B C, McCarty D R, Welch W, Zeevaart J A. 2003. Substrate specificity and kinetics for VP14, a carotenoid cleavage dioxygenase in the ABA biosynthetic pathway. Biochimica et Biophysica Acta (General Subjects), 1619, 9–14.

Shiwachi H, Ayankanmi T, Asiedu R, Onjo M. 2003. Influence of exogenous gibberellin inhibitors on tuber sprouting in yam. Tropical Science, 43, 147–151.

Skelton R L, Yu Q, Srinivasan R, Manshardt R, Moore P H, Ming R. 2006. Tissue differential expression of lycopene β-cyclase gene in papaya. Cell Research, 16, 731–739.

Stupar R M, Bhaskar P B, Yandell B S, Rensink W A, Hart A L, Ouyang S. 2007. Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics, 176, 2055–2067.

Sun L, Yuan B, Zhang M, Wang L, Cui M, Wang Q. 2012. Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and β-carotene contents in tomato fruit. Journal of Experimental Botany, 63, 3097–3108.

Tadmor Y, King S, Levi A, Davis A, Meir A, Wasserman B. 2005. Comparative fruit colouration in watermelon and tomato. Food Research International, 38, 837–841.

Taylor I B, Burbidge A, Thompson A J. 2000. Control of abscisic acid synthesis. Journal of Experimenal Botany, 51, 1563–1574.

Tuan P A, Park N I, Li X, Xu H, Kim H H, Park S U. 2010. Molecular cloning and characterization of phenylalanine ammonia-lyase and cinnamate 4-hydroxylase in the phenylpropanoid biosynthesis pathway in garlic (Allium sativum). Journal of Agricultural and Food Chemistry, 58, 10911–10917.

Welsch R, Arango J, Bär C, Salazar B, Al-Babili S, Beltrán J. 2010. Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a phytoene synthase gene. The Plant Cell, 22, 3348–3356.

Yuan P L, Liu W G, Zhao S J, Lu X Q, Yan Z H, He N. 2012. Lycopene content and expression of phytoene synthase and lycopene β-cyclase genes in tetraploid watermelon. In: Cucurbitaceae 2012 Proceedings of the Xth EUCARPIA Meeting on Genetics and Breeding of Cucurbitaceae. Antalya, Turkey, 15–18 October. University of Cukurova,  Ziraat Fakultesi. pp. 315–324.
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