AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (14.1 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper

Transcriptomics‐based identification and characterization of genes related to sugar metabolism in 'Hongshuijing' pitaya

Zhike Zhanga,1Yemiao Xinga,1Muthusamy Ramakrishnanb,cCanbin ChenaFangfang XieaQingzhu HuaaJianye ChenaRong ZhangaJietang ZhaoaGuibing HuaYonghua Qina( )
State Key Laboratory for Conservation and Utilization of Subtropical Agrobioresources/ Guangdong Provincial Key Laboratory of Postharvest Science of Fruits and Vegetables/Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (South China), Ministry of Agriculture and Rural Affairs, College of Horticulture, South China Agricultural University, Guangzhou 510642, China
Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing 210037, China
Bamboo Research Institute, Nanjing Forestry University, Nanjing 210037, China

1 These authors contributed equally to this work.

Show Author Information

Abstract

Sugar composition not only affects fruit flavor but is also an important determinant of fruit taste and consumer preference. In this study, changes in the sugar content and sugar-metabolizing enzymes were investigated from different sections of various fruit development phases of 'Hongshuijing' pitaya (Hylocereus monacanthus). Genes related to sugar metabolism were also screened by transcriptome analyses. The results indicated that glucose was the major sugar in mature pitaya fruit, and was mainly regulated by vacuolar acid invertase (VAI) and sucrose synthase (SS) (degradative direction). Sugar accumulation varied in pulp between different sections of the pitaya fruit. VAI, neutral invertase (NI) and SS (degradative direction) are crucial enzymes for sugar accumulation in pitaya. The expression of 17 genes related to sucrose metabolism obtained from seven databases [NCBI non-redundant protein database (Nr), NCBI non-redundant nucleotide sequence database (Nt), EuKaryotic Orthologous Groups (KOG), The Protein Families (Pfam), Kyoto Encyclopedia of Genes and Genomes (KEGG), Swiss-prot, and Gene Ontology (GO)] were analyzed in different pitaya pulp sections. HpVAI1 had the highest relative expression level on the 29th day after pollination (DAP). Positive correlations were found between HpVAI1 expression and VAI activity; HpNI4 and NI activity; HpSS2, HpSS5, and SS activity (synthetic direction), indicating that HpVAI1, HpNI4, and HpSS2 and HpSS5 were involved in the regulation of VAI, NI, and SS (synthetic direction), respectively. HpVAI1 and HpNI4 regulated sucrose degradation and the accumulation of glucose and fructose, while HpSS2 and HpSS5 regulated sucrose synthesis. These results suggest that HpVAI1 plays a key role in sugar metabolism during fruit development of 'Hongshuijing' pitaya. The results of this study provide new information about sugar metabolism in pitaya fruit that could help improve fruit quality and the breeding of new cultivars.

References

 

Aslam, M., Deng, L., Wang, X., Wang, Y., Lei, P., Liu, H., Niu, L., Lu, Z., Cui, G., Zeng, W., Wang, Z., 2019. Expression patterns of genes involved in sugar metabolism and accumulation during peach fruit development and ripening. Sci Hortic, 257, 108633.

 

Anur, R.M., Mufithah, N., Sawitri, W.D., Sakakibara, H., Sugiharto, B., 2020. Overexpression of sucrose phosphate synthase enhanced sucrose content and biomass production in transgenic sugarcane. Plants, 9: 200.

 

Basson, C., Groenewald, J., Kossmann, J., Cronjé, C., Bauer, R., 2010. Sugar and acid-related quality attributes and enzyme activities in strawberry fruits: invertase is the main sucrose hydrolysing enzyme. Food Chem, 121: 1156–1162.

 

Chen, C., Wu, P., Xie, F., Sun, L., Xing, Y., Hua, Q., Zhang, Z., Chen, J., Zhao, J., Hu, G., 2018. Breeding of 'Hongguan No. 1' and 'Shuangse No. 1' pitayas with superior quality. HortScience, 53: 404–409.

 

Chen, M., Chen, X., Ci, Z., Shi, Z., 2006. Changes of sugar and acid constituents in apricot during fruit development. Acta Hortic Sin, 33: 805–808 (in Chinese).

 

Deng, S.Y., Mai, Y.T., Niu, J., 2018. Fruit characteristics, soluble sugar compositions and transcriptome analysis during the development of Citrus maxima "seedless", and identification of SUS and INV genes involved in sucrose degradation. Gene, 689: 131–140.

 

García Cruz, L., Dueñas, M., Santos Buelgas, C., Valle Guadarrama, S., Salinas Moreno, Y., 2017. Betalains and phenolic compounds profiling and antioxidant capacity of pitaya (Stenocereus spp.) fruit from two species (S. Pruinosus and S. stellatus). Food Chem, 234: 111–118.

 

Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol, 29: 644–652.

 

Hu, Z.Q., Wang, H.C., Hu, G.B., 2005. Measurement of sugars, organic acids and vitamin C in litchi fruit by high performance liquid chromatography. J Fruit Sci, 5: 34–36.

 

Hua, Q., Chen, C., Zur, N.T., Wang, H., Wu, J., Chen, J., Zhang, Z., Zhao, J., Hu, G., Qin, Y., 2018. Metabolomic characterization of pitaya fruit from three red-skinned cultivars with different pulp colors. Plant Physiol Biochem, 126: 117–125.

 

Huang, S., Lin, H., 2010. Changes in the activities of sugar synthesis enzymes and malate dehydrogenase in Hylocereus undatus fruit during later period of development. J Taiwan Soc Hortic Sci, 56: 81–91.

 

Iqbal, S., Ni, X., Bilal, M.S., Shi, T., Khalil-ur-Rehman, M., Pan, Z., Gao, J., Usman, M., Gao, Z., 2020. Identification and expression profiling of sugar transporter genes during sugar accumulation at different stages of fruit development in apricot. Gene, 742, 144584.

 

Jiang, C.C., Fang, Z.Z., Zhou, D.R., Pan, S.L., Ye, X.F., 2019. Changes in secondary metabolites, organic acids and soluble sugars during the development of plum fruit cv. 'Furongli' (Prunus salicina Lindl). J Sci Food Agric, 99: 1010–1019.

 

King, S.P., Lunn, J.E., Furbank, R.T., 1997. Carbohydrate content and enzyme metabolism in developing canola siliques. Plant Physiol, 114: 153–160.

 

Le Bellec, F., Vaillant, F., Imbert, E., 2006. Pitahaya (Hylocereus spp.): a new fruit crop, a market with a future. Fruits, 61: 237–250.

 

Li, B., Dewey, C.N., 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform, 12: 323.

 

Li, L., Li, N., Jiang, S., 2009. Experimental Guidance of Plant Physiology Module. Science press, Beijing (in Chinese).

 

Li, M., Feng, F., Cheng, L., 2012. Expression patterns of genes involved in sugar metabolism and accumulation during apple fruit development. PLoS ONE, 7: e33055.

 

Lin, Q., Wang, C., Dong, W., Jiang, Q., Wang, D., Li, S., Chen, M., Liu, C., Sun, C., Chen, K., 2015. Transcriptome and metabolome analyses of sugar and organic acid metabolism in Ponkan (Citrus reticulata) fruit during fruit maturation. Gene, 554: 64–74.

 

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.

 

Lowell, C.A., Tomlinson, P.T., Koch, K.E., 1989. Sucrose-metabolizing enzymes in transport tissues and adjacent sink structures in developing citrus fruit. Plant Physiol, 90: 1394–1402.

 

Luo, T., Shuai, L., Liao, L.Y., Li, J., Duan, Z.H., Guo, X.M., Xue, X.Q., Han, D.M., Wu, Z.X., 2019. Soluble acid invertases act as key factors influencing the sucrose/hexose ratio and sugar receding in longan (Dimocarpus longan Lour.) pulp. J Agric Food Chem, 67: 352–363.

 

Manoochehri, H., Hosseini, N.F., Saidijam, M., Taheri, M., Rezaee, H., Nouri, F., 2020. A review on invertase: its potentials and applications. Biocatal Agric Biotechnol, 25, 101599.

 

Montoya-Arroyo, A., Schweiggert, R.M., Pineda-Castro, M.L., Sramek, M., Kohlus, R., Carle, R., Esquivel, P., 2014. Characterization of cell wall polysaccharides of purple pitaya (Hylocereus sp.) pericarp. Food Hydrocoll, 35: 557–564.

 

Moscatello, S., Famiani, F., Proietti, S., Farinelli, D., Battistelli, A., 2011. Sucrose synthase dominates carbohydrate metabolism and relative growth rate in growing kiwifruit (Actinidia deliciosa, cv Hayward). Sci Hortic, 128: 197–205.

 

Ren, R., Yue, X., Li, J., Xie, S., Guo, S., Zhang, Z., 2020. Coexpression of sucrose synthase and the SWEET transporter, which are associated with sugar hydrolysis and transport, respectively, increases the hexose content in Vitis vinifera L. grape berries. Front Plant Sci, 11: 321.

 

Ruan, Y.L., 2014. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol, 65: 33–67.

 

Shammai, A., Petreikov, M., Yeselson, Y., Faigenboim, A., Moy-Komemi, M., Cohen, S., Cohen, D., Besaulov, E., Efrati, A., Houminer, N., Bar, M., Ast, T., Schuldiner, M., Klemens, P.A.W., Neuhaus, E., Baxter, C.J., Rickett, D., Bonnet, J., White, R., Giovannoni, J.J., Levin, I., Schaffer, A., 2018. Natural genetic variation for expression of a SWEET transporter among wild species of tomato determines the hexose composition of ripening tomato fruit. Plant J, 96: 343–357.

 

Shen, L.B., Qin, Y.L., Qi, Z.Q., Niu, Y., Liu, Z.J., Liu, W.X., He, H., Cao, Z.M., Yang, Y., 2019. Genome-wide analysis, expression profile, and characterization of the acid invertase gene family in pepper. Int J Mol Sci, 20: 15.

 

Shivalingamurthy, S.G., Anangi, R., Kalaipandian, S., Glassop, D., King, G.F., Rae, A.L., 2018. Identification and functional characterization of sugarcane invertase Inhibitor (ShINH1): a potential candidate for reducing pre- and post-harvest loss of sucrose in sugarcane. Front Plant Sci, 9: 598.

 

Shuai, L., Li, J., Niu, J., Qian, P., Liu, W., Xue, X., Han, D., Wu, Z., 2016. Sucrose-metabolizing enzymes and their genes in the arils of two Dimocarpus longan cultivars. Biol Plant, 60: 741–748.

 

Smith, A.M., Zeeman, S.C., 2006. Quantification of starch in plant tissues. Nat Protoc, 1: 1342–1345.

 

Song, H., Chu, Q., Yan, F., Yang, Y., Han, W., Zheng, X., 2016. Red pitaya betacyanins protects from diet-induced obesity, liver steatosis and insulin resistance in association with modulation of gut microbiota in mice. J Gastroenterol Hepatol, 31: 1462–1469.

 

Tian, L., Jia, H., Li, C., Fan, P., Xing, Y., Shen, Y., 2012. Sucrose accumulation during grape berry and strawberry fruit ripening is controlled predominantly by sucrose synthase activity. J Hortic Sci Biotechnol, 87: 661–667.

 

Umer, M.J., Safdar, L.B., Gebremeskel, H., Zhao, S., Yuan, P., Zhu, H., Kaseb, M.O., Anees, M., Lu, X., He, N., Gong, C., Liu, W., 2020. Identification of key gene networks controlling organic acid and sugar metabolism during watermelon fruit development by integrating metabolic phenotypes and gene expression profiles. Hortic Res, 7: 193.

 

Wang, C., Wang, Y., Wang, M., Han, H., Luo, Y., Ding, W., Xu, W., Zhong, Y., Huang, H., Qu, S., 2020. Soluble sugars accumulation and related gene expression during fruit development in Cucurbita maxima Duchesne. Sci Hortic, 272, 109520.

 

Wang, H., Huang, H., Huang, X., 2003. Sugar accumulation and related enzyme activities in the litchi fruit of 'Nuomici' and 'Feizixiao'. Acta Hortic Sin, 1: 1–5 (in Chinese).

 

Wang, T., Wright, D., Xu, H., Yang, Y., Zheng, R., Shi, J., Chen, R., Wang, L., 2019. Expression patterns, activities and sugar metabolism regulation of sucrose phosphate synthase, sucrose synthase, neutral invertase and soluble acid invertase in different Goji cultivars during fruit development. Russ J Plant Physiol, 66: 29–40.

 

Wang, Y., Chen, J., Feng, J., Qin, Q., Huang, J., 2015. Overexpression of a loquat (Eriobotrya japonica Lindl.) vacuolar invertase affects sucrose levels and growth. Plant Cell, Tiss Org Cult, 123: 99–108.

 

Wechter, W.P., Levi, A., Harris, K.R., Davis, A.R., Fei, Z.J., Katzir, N., Giovannoni, J.J., Salman-Minkov, A., Hernandez, A., Thimmapuram, J., Tadmor, Y., Portnoy, V., Trebitsh, T., 2008. Gene expression in developing watermelon fruit. BMC Genom, 9: 275.

 

Wei, W., Cheng, M., Ba, L., Zeng, R., Luo, D., Qin, Y., Liu, Z., Kuang, J., Lu, W., Chen, J., 2019. Pitaya, HpWRKY3 is associated with fruit sugar accumulation by transcriptionally modulating sucrose metabolic genes HpINV2 and HpSuSy1. Int J Mol Sci, 20: 1890.

 

Xi, W., Zheng, H., Zhang, Q., Li, W., 2016. Profiling taste and aroma compound metabolism during apricot fruit development and ripening. Int J Mol Sci, 17: 998.

 

Xiao, X., Tang, C., Fang, Y., Yang, M., Zhou, B., Qi, J., Zhang, Y., 2014. Structure and expression profile of the sucrose synthase gene family in the rubber tree: indicative of roles in stress response and sucrose utilization in the laticifers. FEBS J, 281: 291–305.

 

Yamaki, S., 2010. Metabolism and accumulation of sugars translocated to fruit and their regulation. J Jpn Soc Hortic Sci, 79: 1–15.

 

Yan, M.L., Wang, Z.P., Fan, Y., Zhou, M., Sun, P., Shan, S.M., Dai, H.J., 2010. Roles of sucrose-metabolizing enzymes in accumulation of sugars in Cabernet Sauvignon grape fruit. J Fruit Sci, 27: 703–707.

 

Zhang, X.M., Dou, M.A., Yao, Y.L., Du, L.Q., Sun, G.M., Li, J.G., 2011. Sugar accumulation in 'Smooth Cayenne' pineapple fruits in different harvest seasons. Acta Hortic, 902: 193–199.

 

Zhao, Z., Zhang, S., Xu, C., Cheng, K., Liu, A., 2001. Roles of sucrose-metabolizing enzymes in accumulation of sugars in Satsuma mandarin fruit. Acta Hortic Sin, 28: 112–118 (in Chinese).

 

Zhu, Y.J., Komor, E., Moore, P.H., 1997. Sucrose accumulation in the sugarcane stem is regulated by the difference between the activities of soluble acid invertase and sucrose phosphate synthase. Plant Physiol, 115: 609–616.

Horticultural Plant Journal
Pages 450-460
Cite this article:
Zhang Z, Xing Y, Ramakrishnan M, et al. Transcriptomics‐based identification and characterization of genes related to sugar metabolism in 'Hongshuijing' pitaya. Horticultural Plant Journal, 2022, 8(4): 450-460. https://doi.org/10.1016/j.hpj.2021.06.004

370

Views

10

Downloads

17

Crossref

19

Web of Science

18

Scopus

0

CSCD

Altmetrics

Received: 18 February 2021
Revised: 19 May 2021
Accepted: 11 June 2021
Published: 20 August 2021
© 2022 Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS).

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Return