|
|
|
Response of carbohydrate metabolism-mediated sink strength to auxin in shoot tips of apple plants |
SU Jing, CUI Wei-fang, ZHU Ling-cheng, LI Bai-yun, MA Feng-wang, LI Ming-jun |
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 |
|
|
摘要
生长素(吲哚-3-乙酸,IAA)对调节植物碳水化合物水平和生长具有较大的影响,但是它调节植物体内糖分水平的机制却很少受到关注。本研究中,我们发现外源IAA主要通过调节MdSUSY1、MdFRK2、MdHxK1和MdSDH2的转录水平进而改变茎尖中果糖(Fru)、葡萄糖(Glc)和蔗糖(Suc)浓度。此外,我们利用五年生的“Royal Gala”苹果树进一步验证这些基因在调控库强方面的主要作用。结果表明,MdSUSY1、MdFRK2、MdHxK1/3和MdSDH2可能是库强调节的主要贡献基因。综上所述,这些结果为碳水化合物代谢机制的调控提供了新的视角,这将有助于调节库强和产量。
Abstract Auxin (indole-3-acetic acid, IAA) has a considerable impact on the regulation of plant carbohydrate levels and growth, but the mechanism by which it regulates sugar levels in plants has received little attention. In this study, we found that exogenous IAA altered fructose (Fru), glucose (Glc), and sucrose (Suc) concentrations in shoot tips mainly by regulating MdSUSY1, MdFRK2, MdHxK1 and MdSDH2 transcript levels. Additionally, we used 5-year-old ‘Royal Gala’ apple trees to further verify that these genes play primary roles in regulating sink strength. The results showed that MdSUSY1, MdFRK2, MdHxK1/3 and MdSDH2 might be major contributors to sink strength regulation. Taken together, these results provide new insight into the regulation of the carbohydrate metabolism mechanism, which will be helpful for regulating sink strength and yield.
|
Received: 09 August 2020
Accepted: 01 December 2020
|
Fund: This work was supported by the National Natural Science Foundation of China (31672128) and the Chinese Universities Scientific Fund (2452020007). |
About author: SU Jing, E-mail: sujing@nwafu.edu.cn; Correspondence LI Ming-jun, Tel/Fax: +86-538-8246021, E-mail: limingjun@nwsuaf.edu.cn |
Cite this article:
SU Jing, CUI Wei-fang, ZHU Ling-cheng, LI Bai-yun, MA Feng-wang, LI Ming-jun.
2022.
Response of carbohydrate metabolism-mediated sink strength to auxin in shoot tips of apple plants. Journal of Integrative Agriculture, 21(2): 422-433.
|
Agulló-Antón M Á, Sánchez-Bravo J, Acosta M, Druege U. 2011. Auxins or sugars: What makes the difference in the adventitious rooting of stored carnation cuttings? Journal of Plant Growth Regulation, 30, 100–113.
Albacete A A, Martínez-Andújar C, Pérez-Alfocea F. 2014. Hormonal and metabolic regulation of source–sink relations under salinity and drought: From plant survival to crop yield stability. Biotechnology Advances, 32, 12–30.
Archbold D D. 1999. Carbohydrate availability modifies sorbitol dehydrogenase activity of apple fruit. Physiologia Plantarum, 105, 391–395.
Ayre B G. 2011. Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Molecular Plant, 4, 377–394.
Cheng L, Zhou R, Reidel E J, Sharkey T D, Dandekar A M. 2005. Antisense inhibition of sorbitol synthesis leads to up-regulation of starch synthesis without altering CO2 assimilation in apple leaves. Planta, 220, 767–776.
Ciereszko I. 2018. Regulatory roles of sugars in plant growth and development. Acta Societatis Botanicorum Poloniae, 87, 3583.
Claeyssen E, Rivoal J. 2007. Isozymes of plant hexokinase: Occurrence, properties and functions. Phytochemistry, 68, 709–731.
Coleman H D, Beamish L, Reid A, Park J Y, Mansfield S D. 2010. Altered sucrose metabolism impacts plant biomass production and flower development. Transgenic Research, 19, 269–283.
Coleman H D, Samuels A L, Guy R D, Mansfield S D. 2008. Perturbed lignification impacts tree growth in hybrid poplar - A function of sink strength, vascular integrity, and photosynthetic assimilation. Plant Physiology, 148, 1229–1237.
Davies H V, Shepherd L V, Burrell M M, Carrari F, Urbanczyk-Wochniak E, Leisse A, McRae D. 2005. Modulation of fructokinase activity of potato (Solanum tuberosum) results in substantial shifts in tuber metabolism. Plant and Cell Physiology, 46, 1103–1115.
Desnoues E, Génard M, Quilot-Turion B, Baldazzi V. 2018. A kinetic model of sugar metabolism in peach fruit reveals a functional hypothesis of a markedly low fructose-to-glucose ratio phenotype. The Plant Journal, 94, 685–698.
Fajstavr M, Paschová Z, Giagli K, Vavrčík H, Gryc V, Urban J. 2018. Auxin (IAA) and soluble carbohydrate seasonal dynamics monitored during xylogenesis and phloemogenesis in Scots pine. Forest Biogeosciences & Forestry, 11, 553–562.
Fu Q, Cheng L, Guo Y, Turgeon R. 2011. Phloem loading strategies and water relations in trees and herbaceous plants. Plant Physiology, 157, 1518–1527.
Gerber L, Zhang B, Roach M, Rende U, Gorzsás A, Kumar M, Burgert I, Niittylä T, Sundberg B. 2014. Deficient sucrose synthase activity in developing wood does not specifically affect cellulose biosynthesis, but causes an overall decrease in cell wall polymers. New Phytologist, 203, 1220–1230.
German M A, Dai N, Matsevitz T, Hanael R, Petreikov M, Bernstein N, Ioffe M, Shahak Y, Schaffer A A, Granot D. 2003. Suppression of fructokinase encoded by LeFRK2 in tomato stem inhibits growth and causes wilting of young leaves. The Plant Journal, 34, 837–846.
Hansen H, Grossmann K. 2000. Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiology, 124, 1437–1448.
Karve A, Rauh B L, Xia X, Kandasamy M, Meagher R B, Sheen J, Moore B. 2008. Expression and evolutionary features of the hexokinase gene family in Arabidopsis. Planta, 228, 411–425.
Li L Shao T, Yang H, Chen M, Gao X, Long X, Rengel Z. 2017. The endogenous plant hormones and ratios regulate sugar and dry matter accumulation in Jerusalem artichoke in salt-soil. Science of the Total Environment, 578, 40–46.
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.
Li M, Li P, Ma F, Dandekar A M, Cheng L. 2018. Sugar metabolism and accumulation in the fruit of transgenic apple trees with decreased sorbitol synthesis. Horticulture Research, 5, 60.
Li M, Wang S, Liu Y, Zhang Y, Ren M, Liu L, Lu T, Wei H, Wei Z. 2019. Overexpression of PsnSuSy1,2 genes enhances secondary cell wall thickening, vegetative growth, and mechanical strength in transgenic tobacco. Plant Molecular Biology, 100, 215–230.
Liu N. 2019. Effects of IAA and ABA on the immature peach fruit development process. Horticultural Plant Journal, 5, 145–154.
Loescher W H, Marlow G C, Kennedy R A. 1982. Sorbitol metabolism and sink–source interconversions in developing apple leaves. Plant Physiology, 70, 335–339.
Martinelli F, Teo G, Uratsu S L, Podishetty N K, Dandekar A M. 2011. Effects of the silencing of sorbitol dehydrogenase on sugar partitioning in vegetative sinks in apple. European Journal of Horticultural Science, 76, 56.
Morey S R, Hirose T, Hashida Y, Miyao A, Hirochika H, Ohsugi R, Yamagishi J, Aoki N. 2018. Genetic evidence for the role of a rice vacuolar invertase as a molecular sink strength determinant. Rice, 11, 6.
Nonis A, Ruperti B, Falchi R, Casatta E, Enferadi S T, Vizzotto G. 2007. Differential expression and regulation of a neutral invertase encoding gene from peach (Prunus persica): Evidence for a role in fruit development. Physiologia Plantarum, 129, 436–446.
Patrick J W. 1997. Phloem unloading: Sieve element unloading and post-sieve element transport. Annual Review of Plant Biology, 48, 191–222.
Proels R K, Roitsch T. 2009. Extra cellular invertase LIN6 of tomato: A pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. Journal of Experimental Botany, 60, 1555–1567.
Rabot A, Henry C, Ben Baaziz K, Mortreau E, Azri W, Lothier J, Le Gourrierec J. 2012. Insight into the role of sugars in bud burst under light in the rose. Plant and Cell Physiology, 53, 1068–1082.
Reidel E J, Rennie E A, Amiard V, Cheng L, Turgeon R. 2009. Phloem loading strategies in three plant species that transport sugar alcohols. Plant Physiology, 149, 1601–1608.
Ruan Y L. 2012. Signaling role of sucrose metabolism in development. Molecular Plant, 5, 763–765.
Ruan Y L, Jin Y, Yang Y J, Li G J, Boyer J S. 2010. Sugar input, metabolism, and signaling mediated by invertase: Roles in development, yield potential, and response to drought and heat. Molecular Plant, 3, 942–955.
Sagar M, Chervin C, Mila I, Hao Y, Roustan J P, Benichou M, Gibon Y, Biais B, Maury P, Latché A, Pech J C, Bouzayen M, Zouine M. 2013. SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiology, 161, 1362–1374.
Sakr S, Wang M, Dédaldéchamp F, Perez-Garcia M D, Ogé L, Hamama L, Atanassova R. 2018. The sugar-signaling hub: Overview of regulators and interaction with the hormonal and metabolic network. International Journal of Molecular Sciences, 19, 2506.
Shao K, Bai Z, Li M, Yu C, Shao J, Sun Y, Wang R. 2019. Sucrose metabolism enzymes affect sucrose content rather than root weight in sugar beet (Beta vulgaris) at different growth stages. Sugar Tech, 22, 504–517.
Sharma S, Sreenivasulu N, Harshavardhan V T, Seiler C, Sharma S, Khalil Z N, Akhunov E, Sehgal S K, Röder M S. 2010. Delineating the structural, functional and evolutionary relationships of sucrose phosphate synthase gene family II in wheat and related grasses. BMC Plant Biology, 10, 134.
Sheen J. 2014. Master regulators in plant glucose signaling networks. Journal of Plant Biology, 57, 67–79.
Smith H M, Samach A. 2013. Constraints to obtaining consistent annual yields in perennial tree crops. I: Heavy fruit load dominates over vegetative growth. Plant Science, 207, 158–167.
Smith M R, Rao I M, Merchant A. 2018. Source–sink relationships in crop plants and their influence on yield development and nutritional quality. Frontiers in Plant Science, 9, 1889.
Sun J, Zhang J, Larue C T, Huber S C. 2011. Decrease in leaf sucrose synthesis leads to increased leaf starch turnover and decreased RuBP regeneration-limited photosynthesis but not Rubisco-limited photosynthesis in Arabidopsis null mutants of SPSA1. Plant, Cell & Environment, 34, 592–604.
Sun Z, Ma C, Zhou J, Zhu S. 2013. Cloning, expression, purification and assay of sorbitol dehydrogenase from ‘Feicheng’ peach fruit (Prunus persica). Brazilian Archives of Biology and Technology, 56, 531–539.
Teo G, Suzuki Y, Uratsu S L, Lampinen B, Ormonde N, Hu W K, DeJong T, Dandekar A M. 2006. Silencing leaf sorbitol synthesis alters long-distance partitioning and apple fruit quality. Proceedings of the National Academy of Sciences of the United States of America, 103, 18842–18847.
Wang E, Wang J, Zhu X, Hao W, Wang L, Li Q, Zhang L, He W, Lu B, Lin H, Ma H, Zhang G, He Z. 2008. Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nature Genetics, 40, 1370–1374.
Wang X Q, Zheng L L, Lin H, Yu F, Sun L H, Li L M. 2017. Grape hexokinases are involved in the expression regulation of sucrose synthase- and cell wall invertase-encoding genes by glucose and ABA. Plant Molecular Biology, 94, 61–78.
Wang Z, Wei X, Yang J, Li H, Ma B, Zhang K, Zhang Y, Cheng L, Ma F, Li M. 2020. Heterologous expression of the apple hexose transporter MdHT2.2 altered sugar concentration with increasing cell wall invertase activity in tomato fruit. Plant Biotechnology Journal, 18, 540–552.
Xiao W, Sheen J, Jang J C. 2000. The role of hexokinase in plant sugar signal transduction and growth and development. Plant Molecular Biology, 44, 451–461.
Xie Z, Jiang D, Dai T, Jing Q, Cao W. 2004. Effects of exogenous ABA and cytokinin on leaf photosynthesis and grain protein accumulation in wheat ears cultured in vitro. Plant Growth Regulation, 44, 25–32.
Yan W, Wu X, Li Y, Liu G, Cui Z, Jiang T, Ma Q, Luo L, Zhang P. 2019. Cell wall invertase 3 affects cassava productivity via regulating sugar allocation from source to sink. Frontiers in Plant Science, 10, 541.
Yang J, Zhu L, Cui W, Zhang C, Li D, Ma B, Cheng L, Ruan Y, Ma F, Li M. 2018. Increased activity of MdFRK2, a high-affinity fructokinase, leads to upregulation of sorbitol metabolism and downregulation of sucrose metabolism in apple leaves. Horticulture Research, 5, 71.
Yao D, Gonzales-Vigil E, Mansfield S D. 2020. Arabidopsis sucrose synthase localization indicates a primary role in sucrose translocation in phloem. Journal of Experimental Botany, 71, 1858–1869.
Zhang H P, Wu J Y, Tao S T, Wu T, Qi K J, Zhang S J, Wang J Z, Huang W J, Wu J, Zhang S L. 2014. Evidence for apoplasmic phloem unloading in pear fruit. Plant Molecular Biology Reporter, 32, 931–939.
Zhao B, Qi K, Yi X, Chen G, Liu X, Qi X, Zhang S. 2019. Identification of hexokinase family members in pear (Pyrus×bretschneideri) and functional exploration of PbHXK1 in modulating sugar content and plant growth. Gene, 711, 143932.
Zhou R, Cheng L, Dandekar A M. 2006. Down-regulation of sorbitol dehydrogenase and up-regulation of sucrose synthase in shoot tips of the transgenic apple trees with decreased sorbitol synthesis. Journal of Experimental Botany, 57, 3647–3657.
|
No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|