|
Special Issue:
园艺-分子生物合辑Horticulture — Genetics · Breeding
|
|
|
|
| Genome-wide identification, molecular evolution, and expression divergence of the hexokinase gene family in apple |
ZHU Ling-cheng1, SU Jing1, JIN Yu-ru1, ZHAO Hai-yan1, TIAN Xiao-cheng1, ZHANG Chen2, MA Feng-wang1, LI Ming-jun1, MA Bai-quan1 |
1 State Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling 712100, P.R.China
2 Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA |
|
|
|
|
摘要
己糖激酶（HXK）是糖酵解途径中第一个不可逆的催化酶，不仅为植物的生长和发育提供能量，而且还作为响应环境变化的信号分子。但是，HXK基因家族在苹果中的进化模式仍然未知。本研究中，在苹果（Malus×domestica）基因组GDDH13 v1.1中共鉴定出9个HXKs基因，分析了MdHXKs基因的生理和生化特性，外显子-内含子结构，保守基序和顺式元件，亚细胞定位预测结果表明MdHXKs基因主要分布在线粒体、细胞质和细胞核中。基因复制结果显示，全基因组复制（WGD）和片段复制在MdHXKs基因家族扩展中起着至关重要的作用。成对MdHXKs基因的ω值表明，该家族在苹果驯化过程中经历了强烈的纯化选择。此外，对五个亚家族进行了分类，并根据系统进化树分析确定了最近和最老的重复事件，并评估了不同HXKs亚家族之间的进化速率。此外，MdHXKs基因在四个源/库组织和五个苹果果实发育不同阶段的表达模式表明，MdHXKs基因在苹果果实发育和糖积累中起着至关重要的作用。本研究为今后阐明苹果果实发育过程中MdHXKs基因的生物学功能提供了理论基础。
Abstract Hexokinase (HXK) is the first irreversible catalytic enzyme in the glycolytic pathway, which not only provides energy for plant growth and development but also serves as a signaling molecule in response to environmental changes. However, the evolutionary pattern of the HXK gene family in apple remains unknown. In this study, a total of nine HXK genes were identified in the Malus×domestica genome GDDH13 v1.1. The physiological and biochemical properties, exon-intron structures, conserved motifs, and cis-elements of the MdHXK genes were determined. Predicted subcellular localization indicated that the MdHXK genes were mainly distributed in the mitochondria, cytoplasm, and nucleus. Gene duplication revealed that whole-genome duplication (WGD) and segmental duplication played vital roles in MdHXK gene family expansion. The ω values of pairwise MdHXK genes indicated that this family was subjected to strong purifying selection during apple domestication. Additionally, five subfamilies were classified, and recent/old duplication events were identified based on phylogenetic tree analysis. Different evolutionary rates were estimated among the various HXK subfamilies. Moreover, divergent expression patterns of the MdHXK genes in four source-sink tissues and at five different apple fruit developmental stages indicated that they play vital roles in apple fruit development and sugar accumulation. Our study provides a theoretical basis for future elucidation of the biological functions of the MdHXK genes during apple fruit development.
|
|
Received: 18 May 2020
Accepted:
|
| Fund: This work was supported by the National Natural Science Foundation of China (31672128) and the Training Program Foundation for the Young Talents of Northwest A&F University, China (2452020004).
|
|
Corresponding Authors:
Correspondence LI Ming-jun, Tel/Fax: +86-29-87082613, E-mail: limingjun@nwsuaf.edu.cn; MA Bai-quan, Tel/Fax: +86-29-87082613, E-mail: bqma87@nwsuaf.edu.cn
|
| About author: ZHU Ling-cheng, E-mail: zhulingcheng316@nwsuaf.edu.cn; |
Cite this article:
ZHU Ling-cheng, SU Jing, JIN Yu-ru, ZHAO Hai-yan, TIAN Xiao-cheng, ZHANG Chen, MA Feng-wang, LI Ming-jun, MA Bai-quan.
2021.
Genome-wide identification, molecular evolution, and expression divergence of the hexokinase gene family in apple. Journal of Integrative Agriculture, 20(8): 2112-2125.
|
Blanc G, Wolfe K H. 2004. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. The Plant Cell, 16, 1679–1691.
Chagné D, Crowhurst R N, Pindo M, Thrimawithana A, Deng C, Ireland H, Fiers M, Dzierzon H, Cestaro A, Fontana P, Bianco L, Lu A, Storey R, Knäbel M, Saeed M, Montanari S, Kim Y K , Nicolini D, Larger S, Stefani E, et al. 2014. The draft genome sequence of European pear (Pyrus communis L. ‘Bartlett’). PLoS ONE, 9, e92644.
Cheng W, Zhang H, Zhou X, Liu H, Liu Y, Li J, Wang Y. 2011. Subcellular localization of rice hexokinase (OsHXK) family members in the mesophyll protoplasts of tobacco. Biologia Plantarum, 55, 173–177.
Cho J I, Ryoo N, Ko S, Lee S K, Lee J, Jung K H, Lee Y H, Bhoo S H, Winderickx J, An G. 2006. Structure, expression, and functional analysis of the hexokinase gene family in rice (Oryza sativa L.). Planta, 224, 598–611.
Claeyssen E, Rivoal J. 2007. Plant hexokinase isozymes: Occurrence, properties, and functions. Phytochemistry, 68, 709–731.
Daccord N, Celton J M, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H, Bianco L, Micheletti D, Velasco R, Di Pierro E A, Gouzy J, Rees D J G, Guérif P, Muranty H, Durel C E, Laurens F, Lespinasse Y, Gaillard S, Aubourg S, et al. 2017. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nature Genetics, 49, 1099–1106.
Espley R V, Brendolise C, Chagne D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten H J, Gardiner S E, Hellens R P, Allana A C. 2009. Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell, 21, 168–183.
Geng M T, Yao Y, Wang Y L. 2017. Structure, expression, and functional analysis of the hexokinase gene family in cassava. International Journal of Molecular Sciences, 18, 1041.
Granot D. 2007. Role of tomato hexose kinases. Functional Plant Biology, 34, 564–570.
Harrington G N, Bush D R. 2003. The bifunctional role of hexokinase in metabolism and glucose signaling. The Plant Cell, 15, 2493–2496.
Horton P, Nakai K. 1997. Better prediction of protein cellular localization sites with the k nearest neighbors classifier. International Conference on Intelligent Systems for Molecular Biology, 5, 147–152.
Hu D G, Sun C H, Zhang Q Y, An J P, You C X, Hao Y J. 2016. Glucose sensor MdHXK1 phosphorylates and stabilizes MdbHLH3 to promote anthocyanin biosynthesis in apple. PLoS Genetics, 12, e1006273.
Jang J C, Patricia L, Sheen Z J. 1997. Hexokinase as a sugar sensor in higher plants. The Plant Cell, 9, 5–19.
Karve A, Rauh B L, Xia X, Kandasamy M, Meagher R B, Sheen J, Moore B D. 2008. Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta, 228, 411–425.
Karve A A, Moore B D. 2009. Function of Arabidopsis hexokinase-like 1 as a negative regulator of plant growth. Journal of Experimental Botany, 60, 4137–4149.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0. Molecular Biology and Evolution, 33, 1870–1874.
Li J, Ding J, Zhang W, Zhang Y L, Tang P, Chen J Q, Tian D C, Yang S H. 2010. Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Molecular Genetics and Genomics, 283, 427–438.
Li M J, Feng F J, Cheng L L. 2012. Expression patterns of genes involved in sugar metabolism and accumulation during apple fruit development. PLoS ONE, 7, e33055.
Li M J, Li D X, Feng F J, Zhang S, Ma F W, Cheng L L. 2016. Proteomic analysis reveals dynamic regulation of fruit development and sugar and acid accumulation in apple. Journal of Experimental Botany, 67, 5145–5157.
Li M J, Li P M, Ma F W, Cheng L L. 2018. Sugar metabolism and accumulation in the fruit of transgenic apple trees with decreased sorbitol synthesis. Horticulture Research, 5, 60.
Ma B, Liao L, Fang T, Peng Q, Ogutu C, Zhou H, Ma F, Han Y. 2019. A Ma10 gene encoding P-type ATPase is involved in fruit organic acid accumulation in apple. Plant Biotechnology Journal, 17, 674–686.
Ma B Q, Yuan Y Y, Gao M, Qi T H, Li M J, Ma F W. 2018a. Genome-wide identification, molecular evolution, and expression divergence of aluminum-activated malate transporters in apples. International Journal of Molecular Sciences, 19, 2807.
Ma B Q, Yuan Y Y, Gao M, Xing L B, Li C Y, Li M J, Ma F W. 2018b. Genome-wide identification, classification, molecular evolution and expression analysis of malate dehydrogenases in apple. International Journal of Molecular Sciences, 19, 3312.
Moore B, Zhou L, Rolland F, Hall Q, Cheng W H, Liu Y X, Hwang I, Jones T, Sheen J. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science, 300, 332–336.
Panchy N, Lehti-Shiu M, Shiu S H. 2016. Evolution of gene duplication in plant. Plant Physiology, 171, 2294–2316.
Patrick J W, Botha F C, Birch R G. 2013. Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnology Journal, 11, 142–156.
Rensing S A. 2014. Gene duplication as a driver of plant morphogenetic evolution. Current Opinion in Plant Biology, 17, 43–48.
Ruan Y L. 2014. Sucrose metabolism: Gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology, 65, 33–67.
Sun M H, Ma Q J, Hu D G, Zhu X P, You C X, Shu H R, Hao Y J. 2018. The glucose sensor MdHXK1 phosphorylates a tonoplast Na+/H+ exchanger to improve salt tolerance. Plant Physiology, 176, 2977–2990.
Taylor J S, Raes J. 2004. Duplication and divergence: The evolution of new genes and old ideas. Annual Review of Genetics, 38, 615–643.
VanBuren R, Bryant D, Bushakra J M, Vining K J, Edger P P, Rowley E R, Priest H D, Michael T P, Lyons E, Filichkin S A, Dossett M, Finn C E, Bassil N V, Mockler T C. 2016. The genome of black raspberry (Rubus occidentalis). The Plant Journal, 87, 535–547.
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar S K, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, et al. 2010. The genome of the domesticated apple (Malus domestica Borkh.). Nature Genetics, 42, 833–839.
Verde I, Jenkins J, Dondini L, Micali S, Pagliarani G, Vendramin E, Paris R, Aramini V, Gazza L, Rossini L, Bassi D, Troggio M, Shu S, Grimwood J, Tartarini S, Dettori M, Schmutz J. 2017. The Peach v2.0 release: High-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics, 18, 225.
Wan H J, Wu L M, Yang Y J, Zhou G Z, Ruan Y L. 2017. Evolution of sucrose metabolism: The dichotomy of invertases. Trends in Plant Science, 23, 163–177.
Wang D, Zhang Y, Zhang Z, Zhu J, Yu J. 2010. KaKs_Calculator 2.0: A toolkit incorporating gamma-series methods and sliding window strategies. Genomics, Proteomics & Bioinformatics, 8, 77–80.
Wang W, Zhou H, Ma B Q, Owiti A, Korban S S, Han Y P. 2016. Divergent evolutionary pattern of sugar transporter genes is associated with the difference in sugar accumulation between grasses and eudicots. Scientific Reports, 6, 29153.
Wang X Q, Li L M, Yang P P, Gong C L. 2014. The role of hexokinases from grape berries (Vitis vinifera L.) in regulating the expression of cell wall invertase and sucrose synthase genes. Plant Cell Reports, 33, 337–347.
Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S. 2013. The genome of the pear (Pyrus bretschneideri Rehd.). Genome Research, 23, 396–408.
Yang Z. 2007. PAML 4: A program package for phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586–1591.
Yu L, Li J, Li L, Huang Y, Li X, Qiao X, Liu X, Wu J. 2018. Characterisation of the whole-genome wide hexokinase gene family unravels the functional divergence in pear (Pyrus bretschneideri Rehd.). Journal of Horticultural Science & Biotechnology, 93, 244–254.
Zhang Z, Zhang J, Chen Y, Li R, Wang H, Ding L, Wei J. 2014. Isolation, structural analysis, and expression characteristics of the maize (Zea mays L.) hexokinase gene family. Molecular Biology Reports, 41, 6157–6166.
Zhu L, Li B, Wu L, Li H, Wang Z, Wei X, Ma B, Zhang Y, Ma F, Ruan Y L, Li M. 2021. MdERDL6-mediated glucose efflux to the cytosol promotes sugar accumulation in the vacuole through up-regulating TSTs in apple and tomato. Proceedings of the National Academy of Sciences of the United States of America, 118, e2022788118. |
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
