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A glucuronokinase gene in Arabidopsis, AtGlcAK, is involved in drought tolerance by modulating sugar metabolism

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Abstract

Arabidopsis glucuronokinase (AtGlcAK), as a member of the GHMP kinases family, is implicated in the de novo synthesis of UDP-glucuronic acid (UDP-GlcA) by the myo-inositol oxygenation pathway. In this study, two T-DNA insertion homozygous mutants of AtGlcAK, atglcak-1 and atglcak-2, were identified. AtGlcAK was highly expressed in roots and flowers. There was reduced primary root elongation and lateral root formation in atglcak mutants under osmotic stress. The atglcak mutants displayed enhanced stomatal opening in response to abscisic acid (ABA), elevated water loss and impaired drought tolerance. Under water stress, the accumulation of reducing and soluble sugars was reduced in atglcak mutants, and the metabolism of glucose and sucrose was affected by the synthetic pathway of UDP-GlcA. Furthermore, a reduced level of starch in atglcak mutants was observed under normal conditions. The phylogenetic analysis suggested that GlcAK was conserved in numerous dicots and monocots plants. In short, AtGlcAK mutants displayed hypersensitivity to ABA and reduced root development under water stress, rendering the plants more susceptible to drought stress.

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References

  • Adney B, Baker J (1996) NREL technical report NREL/TP-510-42628, 1-8

  • Aubert Y, Vile D, Pervent M, Aldon D, Ranty B, Simonneau T, Vavasseur A, Galaud JP (2010) RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 51:1975–1987

    Article  CAS  PubMed  Google Scholar 

  • Bengough AG, McKenzie BM, Hallett PD, Valentine TA (2011) Root elongation, water stress, and mechanical impedance, a review of limiting stresses and beneficial root tip traits. J Exp Bot 62:59–68

    Article  CAS  PubMed  Google Scholar 

  • Caspar T, Lin TP, Kakefuda G, Benbow L, Preiss J, Somerville C (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol 95:1181–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signalling of water shortage. Plant J 52:167–174

    Article  CAS  PubMed  Google Scholar 

  • Conrad M, Schothorst J, Kankipati HN, Van Zeebroeck G, Rubio-Texeira M, Thevelein JM (2014) Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 38:254–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coruzzi GM, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125:61–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J 26:89–100

    Article  CAS  PubMed  Google Scholar 

  • Dai N, Schaffer A, Petreikov M, Shahak Y, Giller Y, Ratner K, Levine A, Granot D (1999) Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell 11:1253–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubey RS, Singh AK (1999) Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants. Biol Plant 42:233–239

    Article  CAS  Google Scholar 

  • Endo A, Sawada Y, Takahashi H, Okamoto M, Ikegami K, Koiwai H, Seo M, Toyomasu T, Mitsuhashi W, Shinozaki K, Nakazono M, Kamiya Y, Koshiba T, Nambara E (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147:1984–1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eyéghé-Bickong HA, Alexandersson EO, Gouws LM, Young PR, Vivier MA (2012) Optimisation of an HPLC method for the simultaneous quantification of the major sugars and organic acids in grapevine berries. J Chromatogr B 885-886: 43-9

  • Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci U S A 106:8380–8385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garlock RJ, Wong YS, Balan V, Dale BE (2012) AFEX pretreatment and enzymatic conversion of blacklocust (Robinia pseudoacacia L.) to soluble sugars.Bioenerg Res 5:306–318

  • Geserick C, Tenhaken R (2013) UDP-sugar pyrophosphorylase is essential for arabinose and xylose recycling, and is required during vegetative and reproductive growth in Arabidopsis. Plant J 74:239–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102

    Article  CAS  PubMed  Google Scholar 

  • Gill PK, Sharma AD, Singh P, Bhullar SS (2001) Effect of various abiotic stresses on the growth soluble sugars and water relations of sorghum seedlings grown in light and darkness. Bulg J Plant Physiol 27:72–84

    CAS  Google Scholar 

  • Garlock RJ, Wong YS, Balan V, Dale BE (2012) AFEX pretreatment and enzymatic conversion of black locust (Robinia pseudoacacia L.) to soluble sugars. BioEnergy Research 5(2):306–318

  • Hansen J, Moller I (1975) Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Anal Biochem 68:87–94

    Article  CAS  PubMed  Google Scholar 

  • Harper AD, Bar-Peled M (2002) Biosynthesis of UDP-xylose. Cloning and characterization of a novel Arabidopsis gene family, UXS, encoding soluble and putative membrane-bound UDP-glucuronic acid decarboxylase isoforms. Plant Physiol 130:2188–2198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Holden HM, Thoden JB, Timson DJ, Reece RJ (2004) Galactokinase, structure, function and role in type II galactosemia. Cell Mol Life Sci 61:2471–2484

    Article  CAS  PubMed  Google Scholar 

  • Kalckar HM, Braganca B, Munch-Petersen HM (1953) Uridyl transferases and the formation of uridine diphosphogalactose. Nature 172:1038

    Article  CAS  PubMed  Google Scholar 

  • Kelly G, Moshelion M, David-Schwartz R, Halperin O, Wallach R, Attia Z, Belausov E, Granot D (2013) Hexokinase mediates stomatal closure. Plant J 75:977–988

    Article  CAS  PubMed  Google Scholar 

  • Koch K (2004) Sucrose metabolism, regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  CAS  PubMed  Google Scholar 

  • Kollist H, Nuhkat M, Roelfsema MR (2014) Closing gaps, linking elements that control stomatal movement. New Phytol 203:44–62

    Article  CAS  PubMed  Google Scholar 

  • Kotake T, Hojo S, Yamaguchi D, Aohara T, Konishi T, Tsumuraya Y (2007) Properties and physiological functions of UDP-sugar pyrophosphorylase in Arabidopsis. Biosci Biotechnol Biochem 71:761–771

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2007) Interactive Tree Of Life iTOL, an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wang XQ, Watson MB, Assmann SM (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287:300–303

    Article  CAS  PubMed  Google Scholar 

  • Loewus FA, Loewus MW (1983) myo-Inositol, its biosynthesis and metabolism. Annu Rev Plant Physiol 34:137–161

    Article  CAS  Google Scholar 

  • Moreno-Herrero F, Herrero P, Colchero J, Baró AM, Moreno F (1999) Analysis by atomic force microscopy of Med8 binding to cis-acting regulatory elements of the SUC2 and HXK2 genes of saccharomyces cerevisiae. FEBS Lett 459:427–432

    Article  CAS  PubMed  Google Scholar 

  • Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohtsubo K, Marth JD (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126:855–867

    Article  CAS  PubMed  Google Scholar 

  • Pieslinger AM, Hoepflinger MC, Tenhaken R (2010) Cloning of Glucuronokinase from Arabidopsis thaliana, the last missing enzyme of the myo-inositol oxygenase pathway to nucleotide sugars. J Biol Chem 285:2902–2910

    Article  CAS  PubMed  Google Scholar 

  • Prado FE, Boero C, Gallardo M, Gonzalez JA (2000) Effectof NaCl on germination, growth and soluble sugar content inChenopodium quinoa willd seeds. Bot Bull Acad Sin 41:27–34

  • Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling. The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD http//www.aspb.org/publications/arabidopsis

  • Rathinasabapathi B (2000) Metabolic engineering for stress tolerance, installing osmoprotectant synthesis pathways. Ann Bot 86:709–716

    Article  CAS  Google Scholar 

  • Reiter WD, Vanzin GF (2001) Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant Mol Biol 47:95–113

    Article  CAS  PubMed  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants, conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Rosa M, Hilal M, González JA, Prado FE (2009) Low-temperature effect on enzyme activities involved in sucrose-starch partitioning in salt-stressed and salt-acclimated cotyledons of quinoa Chenopodium quinoa Willd. seedlings. Plant Physiol Biochem 47:300–307

    Article  CAS  PubMed  Google Scholar 

  • Ruan YL (2014) Sucrose metabolism, gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67

    Article  CAS  PubMed  Google Scholar 

  • Roychoudhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method, a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874

    Article  CAS  PubMed  Google Scholar 

  • Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247

    Article  CAS  PubMed  Google Scholar 

  • Skillman JB, Griffin KL, Earll S, Kusama M (2011) Photosynthetic productivity: can plants do better? In: Piraján JCM (ed) Thermodynamics—systems in equilibrium andthermodynamics of abiotic stress and stress tolerance of cultivated plants.InTech 2011, pp 35–68

  • Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) Functional characterization of the Arabidopsis AtSUC2 Sucrose/H+ symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol 148:200–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stitt M, Krappe A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition. The physiological and molecular background. Plant Cell Environ 22:583–621

    Article  CAS  Google Scholar 

  • Strand A, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, Stitt M (1999) Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5, molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293

    Article  PubMed  PubMed Central  Google Scholar 

  • Thibodeaux CJ, Melançon CE, Liu HW (2007) Unusual sugar biosynthesis and natural product glycodiversification. Nature 446:1008–1016

    Article  CAS  PubMed  Google Scholar 

  • Tiessen A, Padilla-Chacon D (2013) Subcellular compartmentation of sugar signaling, links among carbon cellular status, route of sucrolysis, sink-source allocation, and metabolic partitioning. Front Plant Sci 3:306

    Article  PubMed  PubMed Central  Google Scholar 

  • Tognetti JA, Pontis HG, Martínez-Noël GM (2013) Sucrose signaling in plants, A world yet to be explored. Plant Signal Behav 8, e23316

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94

    Article  CAS  PubMed  Google Scholar 

  • Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483

  • Zeller G, Henz SR, Widmer CK, Sachsenberg T, Rätsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068–1082

    Article  CAS  PubMed  Google Scholar 

  • Zhao Q, Yu D, Chang H, Guo X, Yuan C, Hu S, Zhang C, Wang P, Wang Y (2013) Regulation and function of Arabidopsis AtGALK2 gene in abscisic acid response signaling. Mol Biol Rep 40:6605–6612

    Article  CAS  Google Scholar 

  • Zheng Z, Xu X, Crosley RA, Greenwalt SA, Sun Y, Blakeslee B, Wang L, Ni W, Sopko MS, Yao C, Yau K, Burton S, Zhuang M, McCaskill DG, Gachotte D, Thompson M, Greene TW (2010) The protein kinase SnRK2.6 mediates the regulation of sucrose metabolism and plant growth in Arabidopsis. Plant Physiol 153:99–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was supported by grants from the National Key Laboratory of Plant Molecular Genetics (2015), the National Natural Science Foundation of China (31540064, 31071076 and 30871325), the Ph.D. Programs Foundation of Ministry of Education of China (20130161110005), Hunan Provincial Innovation Foundation For Postgraduate (CX2015B073, CX2016B097), and Key Research & Development project of Hunan Provincial Department of Science and Technology support (2016WK2003).

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    1. School of Biology, Hunan University, Changsha, 410082, People’s Republic of China

      Wenjun Xiao, Shuai Hu, Runyu Yao, Jingru Luo, Congying Yuan, Hongping Chang, Cheng Zhang, Ji Huang, Jinyan Li, Shucan Liu, Meiling Li & Xinhong Guo

    2. Hunan Agricultural University, Changsha, 410128, People’s Republic of China

      Xiaoxun Zhou

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    1. Wenjun Xiao
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    Correspondence to Xinhong Guo.

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    Wenjun Xiao and Shuai Hu contributed equally to this work.

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    Supplemental Fig. 1

    a Identification of T-DNA events in the two mutant lines. LP/RP was Left/Right genomic primer. LB was Left border primer of the T-DNA insertion. M indicated DNA maker III. b Sequencing of the insertional site. The green and blue boxes meant the T-DNA insertional sites of atglcak-1 and atglcak-2, respectively. The fragment marked in red lower cases was the UTR region. ATG was the star codon of AT3G01640. c Expression analysis of AtGlcAK and AtGALK2 in WT and mutant plants under drought condition. (JPEG 1.13 MB)

    Supplemental Fig. 2

    a Parameter of rosette leaves (RLs). Long axis was shown in black and short axis in gray. b Weight of shoots harvested from 30-day-old plants. Values are means ± SD. Asterisks indicated statistically significant differences compared with WT (Student’s t test,*P < 0.05, **P < 0.01). (JPEG 111 KB)

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    Xiao, W., Hu, S., Zhou, X. et al. A glucuronokinase gene in Arabidopsis, AtGlcAK, is involved in drought tolerance by modulating sugar metabolism. Plant Mol Biol Rep 35, 298–311 (2017). https://doi.org/10.1007/s11105-017-1023-5

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