Guard cells on the leaf epidermis regulate stomatal opening for gas exchange between plants and the atmosphere, allowing a balance between photosynthesis and transpiration. Given that guard cells possess several characteristics of sink tissues, their metabolic activities should largely depend on mesophyll-derived sugars. Early biochemical studies revealed sugar uptake into guard cells. However, the transporters that are involved and their relative contribution to guard cell function are not yet known. Here, we identified the monosaccharide/proton symporters Sugar Transport Protein 1 and 4 (STP1 and STP4) as the major plasma membrane hexose sugar transporters in the guard cells of Arabidopsis thaliana. We show that their combined action is required for glucose import to guard cells, providing carbon sources for starch accumulation and light-induced stomatal opening that are essential for plant growth. These findings highlight mesophyll-derived glucose as an important metabolite connecting stomatal movements with photosynthesis.

Department of Plant and Microbial Biology University of Zürich Zürich Switzerland

Institute of Integrative Biology ETH Zürich Zürich Switzerland

Photon Systems Instruments Drasov Czech Republic

Zobrazit více v PubMed

Alonso M, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R et al (2003) Genome‐wide insertional mutagenesis of Arabidopsis thaliana . Science 301: 653–657 PubMed

Amodeo G, Talbott LD, Zeiger E (1996) Use of potassium and sucrose by onion guard cells during a daily cycle of osmoregulation. Plant Cell Physiol 37: 575–579

Awlia M, Nigro A, Fajkus J, Schmöckel SM, Negrão S, Santelia D, Trtílek M, Tester M, Julkowska MM, Panzarová K (2016) High‐throughput non‐destructive phenotyping of traits that contribute to salinity tolerance in Arabidopsis thaliana . Front Plant Sci 7: 1414 PubMed PMC

Azoulay‐Shemer T, Bagheri A, Wang C, Palomares A, Stephan AB, Kunz HH, Schroeder JI (2016) Starch biosynthesis in guard cells but not in mesophyll cells is involved in CO2‐induced stomatal closing. Plant Physiol 171: 788–798 PubMed PMC

Bates GW, Rosenthal DM, Sun J, Chattopadhyay M, Peffer E, Yang J, Ort DR, Jones AM (2012) A comparative study of the Arabidopsis thaliana guard‐cell transcriptome and its modulation by sucrose. PLoS ONE 7: e49641 PubMed PMC

Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al‐Rasheid KAS, Sonnewald S, Sonnewald U, Kneitz S, Lachmann N et al (2013) The stomatal response to reduced relative humidity requires guard cell‐autonomous ABA synthesis. Curr Biol 23: 53–57 PubMed

Boorers KJ, Loo DDF, Wright EM (1994) Steady‐state and presteady‐state kinetics of the H+/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes. J Biol Chem 269: 20417–20424 PubMed

Büttner M, Sauer N (2000) Monosaccharide transporters in plants: structure, function and physiology. Biochim Biophys Acta 1465: 263–274 PubMed

Büttner M (2010) The Arabidopsis sugar transporter (AtSTP) family: an update. Plant Biol 12: 35–41 PubMed

Chen L‐Q, Cheung LS, Feng L, Tanner W, Frommer WB (2015) Transport of sugars. Annu Rev Biochem 84: 865–894 PubMed

Daloso DM, Antunes WC, Pinheiro DP, Waquim JP, Araújo WL, Loureiro ME, Fernie AR, Williams TCR (2015) Tobacco guard cells fix CO2 by both RubisCO and PEPcase whilst sucrose acts as a substrate during light induced stomatal opening. Plant, Cell Environ 38: 2353–2371 PubMed

Daloso DM, dos Anjos L, Fernie AR (2016a) Roles of sucrose in guard cell regulation. New Phytol 211: 809–818 PubMed

Daloso DM, Williams TCR, Antunes WC, Pinheiro DP, Müller C, Loureiro ME, Fernie AR (2016b) Guard cell‐specific upregulation of sucrose synthase 3 reveals that the role of sucrose in stomatal function is primarily energetic. New Phytol 209: 1470–1483 PubMed

Daloso DM, Medeiros DB, dos Anjos L, Yoshida T, Araújo WL, Fernie AR (2017) Metabolism within the specialized guard cells of plants. New Phytol 216: 1018–1033 PubMed

Dittrich P, Raschke K (1977) Uptake and metabolism of carbohydrates by epidermal tissue. Planta 134: 83–90 PubMed

Flütsch S, Distefano L, Santelia D (2018) Quantification of starch in guard cells of Arabidopsis thaliana . Bio‐Protocol 8: e2920 PubMed PMC

Flütsch S, Wang Y, Takemiya A, Vialet‐Chabrand S, Klajchova M, Nigro A, Hills A, Lawson T, Blatt MR, Santelia D (2020) Guard cell starch degradation yields glucose for rapid stomatal opening in Arabidopsis . Pant Cell 32: 1–20 PubMed PMC

Hamill S, Cloherty EK, Carruthers A (1999) The human erythrocyte sugar transporter presents two sugar import sites. Biochemistry 38: 16974–16983 PubMed

Horrer D, Flütsch S, Pazmino D, Matthews JSA, Thalmann M, Nigro A, Leonhardt N, Lawson T, Santelia D (2016) Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening. Curr Biol 26: 362–370 PubMed

Inoue S, Kinoshita T (2017) Blue light regulation of stomatal opening and the plasma membrane H+‐ATPase. Plant Physiol 174: 531–538 PubMed PMC

Jezek M, Blatt MR (2017) The membrane transport system of the guard cell and its integration for stomatal dynamics. Plant Physiol 174: 487–519 PubMed PMC

Jung B, Ludewig F, Schulz A, Meißner G, Wöstefeld N, Flügge UI, Pommerrenig B, Wirsching P, Sauer N, Koch W et al (2015) Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nat Plants 1: 14001 PubMed

Kang Y, Outlaw WH, Andersen PC, Fiore GB (2007) Guard‐cell apoplastic sucrose concentration–a link between leaf photosynthesis and stomatal aperture size in the apoplastic phloem loader Vicia faba L. Plant, Cell Environ 30: 551–558 PubMed

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 PubMed

Lawson T, Vialet‐Chabrand S (2019) Speedy stomata, photosynthesis and plant water use efficiency. New Phytol 221: 93–98 PubMed

Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16: 596–615 PubMed PMC

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real‐time quantitative PCR and the 2‐ΔΔCT method. Methods 25: 402–408 PubMed

Lu P, Zhang SQ, Outlaw WH, Riddle KA (1995) Sucrose: a solute that accumulates in the guard‐cell apoplast and guard‐cell symplast of open stomata. FEBS Lett 362: 180–184 PubMed

Lu P, Outlaw WH Jr, Smith BG, Freed GA (1997) A new mechanism for the regulation of stomatal aperture size in intact leaves. Plant Physiol 114: 109–118 PubMed PMC

Lugassi N, Kelly G, Fidel L, Yaniv Y, Attia Z, Levi A, Alchanatis V, Moshelion M, Raveh E, Carmi N et al (2015) Expression of Arabidopsis hexokinase in citrus guard cells controls stomatal aperture and reduces transpiration. Front Plant Sci 6: 1–11 PubMed PMC

Medeiros DB, de Souza LP, Antunes WC, Araújo WL, Daloso DM, Fernie AR (2018) Sucrose breakdown within guard cells is a substrate for glycolysis and glutamine biosynthesis during light‐induced stomatal opening. Plant J 94: 583–594 PubMed

Merlot S, Mustilli A‐C, Genty B, North H, Lefebvre V, Sotta B, Vavasseur A, Giraudat J (2002) Use of infrared thermal imaging to isolate Arabidopsis mutants defective in stomatal regulation. Plant J 30: 601–609 PubMed

Norholm MHH, Nour‐Eldin HH, Brodersen P, Mundy J, Halkier BA (2006) Expression of the Arabidopsis high‐affinity hexose transporter STP13 correlates with programmed cell death. FEBS Lett 580: 2381–2387 PubMed

Outlaw WH, Manchester J (1979) Guard cell starch concentration quantitatively related to stomatal aperture. Plant Physiol 64: 79–82 PubMed PMC

Outlaw WH, Manchester J, DiCamelli CA, Randall DD, Rapp B, Veith GM (1979) Photosynthetic carbon reduction pathway is absent in chloroplasts of Vicia faba guard cells. Proc Natl Acad Sci USA 76: 6371–6375 PubMed PMC

Outlaw WH (1989) Critical examination of the quantitative evidence for and against photosynthetic CO2 fixation by guard cells. Physiol Plant 77: 275–281

Outlaw WH, De Vlieghere‐He X (2001) Transpiration rate. An important factor controlling the sucrose content of the guard cell apoplast of broad bean. Plant Physiol 126: 1716–1724 PubMed PMC

Penfield S, Clements S, Bailey KJ, Gilday AD, Leegood RC, Gray JE, Graham IA (2012) Expression and manipulation of phosphoenolpyruvate carboxykinase 1 identifies a role for malate metabolism in stomatal closure. Plant J 69: 679–688 PubMed

Poffenroth M, Green DB, Tallman G (1992) Sugar concentrations in guard cells of Vicia faba illuminated with red or blue light: analysis by high performance liquid chromatography. Plant Physiol 98: 1460–1471 PubMed PMC

Poschet G, Hannich B, Büttner M (2010) Identification and characterization of AtSTP14, a novel galactose transporter from Arabidopsis . Plant Cell Physiol 51: 1571–1580 PubMed

R Core Team (2015) R: a language and environment for statistical computing. Vienna, Austria: R Core Team;

Reckmann U, Scheibe R, Raschke K (1990) Rubisco activity in guard cells compared with the solute requirement for stomatal opening. Plant Physiol 92: 246–253 PubMed PMC

Reddy AR, Das VSR (1986) Stomatal movement and sucrose uptake by guard cell protoplasts of Commelina benghalensis L. Plant Cell Physiol 27: 1565–1570

Reinders A, Schulze W, Kühn C, Barker L, Schulz A, Ward JM, Frommer WB (2002) Protein‐protein interactions between sucrose transporters of different affinities colocalized in the same enucleate sieve element. Plant Cell 14: 1567–1577 PubMed PMC

Ritte G, Rosenfeld J, Rohrig K, Raschke K (1999) Rates of sugar uptake by guard cell protoplasts of Pisum sativum L. related to the solute requirement for stomatal opening. Plant Physiol 121: 647–655 PubMed PMC

Robaina‐Estévez S, Daloso DM, Zhang Y, Fernie AR, Nikoloski Z (2017) Resolving the central metabolism of Arabidopsis guard cells. Sci Rep 7: 1–13 PubMed PMC

Rottmann T, Zierer W, Subert C, Sauer N, Stadler R (2016) STP10 encodes a high‐affinity monosaccharide transporter and is induced under low‐glucose conditions in pollen tubes of Arabidopsis . J Exp Bot 67: 2387–2399 PubMed PMC

Rottmann TM, Fritz C, Sauer N, Stadler R (2018a) Glucose uptake via STP transporters inhibits in vitro pollen tube growth in a HEXOKINASE1‐ dependent manner in Arabidopsis thaliana . Plant Cell 30: 2057–2081 PubMed PMC

Rottmann TM, Klebl F, Schneider S, Kischka D, Rüscher D, Sauer N, Stadler R (2018b) Sugar transporter STP7 specificity for L‐arabinose and D‐xylose contrasts with the typical hexose transporters STP8 and STP12. Plant Physiol 176: 2330–2350 PubMed PMC

Rouse JW, Hass RH, Schell JA, Deering DW (1974) Monitoring vegetation systems in the great plains with ERTS. Third Earth Resour Technol Satell Symp 1: 309–317

Rui Y, Anderson CT (2016) Functional analysis of cellulose and xyloglucan in the walls of stomatal guard cells of Arabidopsis thaliana . Plant Physiol 170: 1398–1419 PubMed PMC

Santelia D, Lawson T (2016) Rethinking guard cell metabolism. Plant Physiol 172: 1371–1392 PubMed PMC

Sauer N, Friedländer K, Gräml‐Wicke U (1990) Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana . EMBO J 9: 3045–3050 PubMed PMC

Schofield RA, Bi Y‐M, Kant S, Rothstein SJ (2009) Over‐expression of STP13, a hexose transporter, improves plant growth and nitrogen use in Arabidopsis thaliana seedlings. Plant, Cell Environ 32: 271–285 PubMed

Schulz A, Beyhl D, Marten I, Wormit A, Neuhaus E, Poschet G, Büttner M, Schneider S, Sauer N, Hedrich R (2011) Proton‐driven sucrose symport and antiport are provided by the vacuolar transporters SUC4 and TMT1/2. Plant J 68: 129–136 PubMed

Sherson SM, Hemmann G, Wallace G, Forbes S, Germain V, Stadler R, Bechtold N, Sauer N, Smith SM (2000) Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. Plant J 24: 849–857 PubMed

Stadler R, Bu M, Ache P, Hedrich R, Ivashikina N, Melzer M, Shearson SM, Smith SM, Sauer N, Germany RS (2003) Diurnal and light‐regulated expression of AtSTP1 in guard cells of Arabidopsis . Plant Physiol 133: 528–537 PubMed PMC

Talbott LD, Zeiger E (1993) Sugar and organic acid accumulation in guard cells of Vicia faba in response to red and blue light. Plant Physiol 102: 1163–1169 PubMed PMC

Thalmann M, Pazmino D, Seung D, Horrer D, Nigro A, Meier T, Kölling K, Pfeifhofer WH, Zeeman SC, Santelia D (2016) Regulation of leaf starch degradation by abscisic acid is important for osmotic stress tolerance in plants. Plant Cell 28: 1860–1878 PubMed PMC

Truernit E, Schmid J, Epple P, Illig J, Sauer N (1996) The sink‐specific and stress‐regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8: 2169–2182 PubMed PMC

Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long‐distance signalling in Arabidopsis . Plant J 32: 255–262 PubMed

Wang R‐S, Pandey S, Li S, Gookin TE, Zhao Z, Albert R, Assmann SM (2011) Common and unique elements of the ABA‐regulated transcriptome of Arabidopsis guard cells. BMC Genom 12: 216–222 PubMed

Wille AC, Lucas WJ (1984) Ultrastructural and histochemical studies on guard cells. Planta 160: 129–142 PubMed

Yamada K, Kanai M, Osakabe Y, Ohiraki H, Shinozaki K, Yamaguchi‐Shinozaki K (2011) Monosaccharide absorption activity of Arabidopsis roots depends on expression profiles of transporter genes under high salinity conditions. J Biol Chem 286: 43577–43586 PubMed PMC

Yamada K, Saijo Y, Nakagami H, Takano Y (2016) Regulation of sugar transporter activity for antibacterial defense in Arabidopsis . Science 354: 1427–1430 PubMed

Yang Y, Costa A, Leonhardt N, Siegel RS, Schroeder JI (2008) Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool. Plant Methods 4: 6 PubMed PMC

Differential expression and localization of expansins in Arabidopsis shoots: implications for cell wall dynamics and drought tolerance

Zobrazit více v PubMed

RefSeq
AT3G18780, AT4G17090, AT5G46240, AT1G08810, AT1G11260, AT3G19930, AT5G26340, AT1G71880, AT2G02860