Guard Cell Metabolism

Abstract

Guard cells are found in leaf epidermis as a pair of cells surrounding the stomatal pore. Stomatal aperture is regulated by the metabolism of guard cells according to the prevailing environmental condition. Guard cell metabolism is thus adapted to support stomatal movement, which demands a high control of osmolytes content within the cell as well as the need to balance the exchange of ions and metabolites between the cytoplasm and the apoplastic space. Guard cells have several characteristics of sink cells. This is probably an alternative given the low photosynthetic rate and the few number of chloroplasts found in these cells. The glycolysis, the tricarboxylic acid cycle and the degradation of starch and lipids seem to be activated in the light to support stomatal opening. This indicates that guard cell metabolism is differentially regulated compared to mesophyll cells. The particularities of guard cell metabolism are reviewed here.

Key Concepts

  • Stomatal aperture controls water use efficiency by modulating CO2 and H2O exchanges between the leaf and the atmosphere.
  • Changes in osmolyte concentration within guard cells regulate stomatal aperture.
  • Signals from mesophyll cells are known to alter stomatal movements.
  • Malate imported from mesophyll cells or produced within guard cells is involved on stomatal movement regulation.
  • Guard cells have several characteristics of sink cells.
  • It seems likely that photosynthesis in guard cell chloroplasts is mainly related to provide ATP and NADPH required for turgor control rather than producing carbohydrates.
  • Lipids, starch and sucrose are degraded during light‐induced stomatal opening.
  • Mitochondria metabolism is important to maintain guard cell energetic demands.

Keywords: glycolysis; malate; photosynthesis; respiration; stomatal movement; sucrose; tricarboxylic acid cycle

Figure 1. (a) Guard cell metabolism during day and night conditions. During the day, guard cell photosynthesis and mitochondria provide the ATP needed to maintain the activity of plasma membrane H+‐ATPases, which is important to create a H+ gradient across guard cell plasma membrane. This H+ gradient is dissipated by the transport of ions between the apoplastic space and the symplast of guard cells during stomatal opening. Phototropins, blue light receptors located in plasma membrane of guard cells, stimulate H+‐ATPase pump. Phototropin signalling is also a mechanism to stimulate starch and lipid (TAG) degradation. By contrast to mesophyll cells, in which respiration is light inhibited, guard cells seem to degrade starch, lipids and sucrose to sustain mitochondrial metabolism and glutamine biosynthesis. In this vein, guard cells have higher anaplerotic CO2 fixation mediated by PEPc, when compared to mesophyll cells. Given the low RubisCO‐mediated photosynthetic capacity of guard cells, sucrose may also be imported from neighbouring mesophyll cells. Therefore, sucrose is a putative signal from mesophyll cells that connects mesophyll photosynthetic process with stomatal movement. Another important metabolite for guard cell metabolism is malate, which can be imported from mesophyll cells and synthesised within guard cells from starch breakdown and PEPc fixation. Malate accumulation in the vacuole acts as a counter‐ion of K+. During the night, the content of guard cell osmolyte molecules such as malate and sugars seems to be converted into starch. Furthermore, sucrose accumulation at the apoplastic space and its degradation within guard cells has been reported as mechanisms to induce stomatal closure. Thus, the transport of sucrose mesophyll cells may also contribute to stomatal closure during stomatal closure conditions. However, these hypotheses have yet to be tested. (b) Diel course of starch synthesis and degradation in both mesophyll and guard cells. Whilst mesophyll cells have a linear pattern of starch synthesis in the light and starch degradation in the night, guard cells linearly degrade starch at the beginning of the diel course and accumulate starch in the rest of the day and during the beginning of the night. For this, different isoforms of AMY and BAM enzymes seems to be involved in starch degradation in mesophyll and guard cells (a).
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References

dos Anjos L , Pandey PK , Moraes TA , et al. (2018) Feedback regulation by trehalose 6‐phosphate slows down starch mobilization below the rate that would exhaust starch reserves at dawn in Arabidopsis leaves. Plant Direct 2: e00078.

Antunes WC , de Menezes Daloso D , Pinheiro DP , Williams TCR and Loureiro ME (2017) Guard cell‐specific down‐regulation of the sucrose transporter SUT1 leads to improved water use efficiency and reveals the interplay between carbohydrate metabolism and K+ accumulation in the regulation of stomatal opening. Environmental and Experimental Botany 135: 73–85.

Araújo WL , Nunes‐Nesi A , Osorio S , et al. (2011) Antisense inhibition of the iron‐sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid–mediated effect on stomatal aperture. The Plant Cell 23: 600–627.

Aubry S , Aresheva O , Reyna‐Llorens I , et al. (2016) A specific transcriptome signature for guard cells from the C4 plant Gynandropsis gynandra . Plant Physiology 170: 1345–1357.

Azoulay‐Shemer T , Palomares A , Bagheri A , et al. (2015) Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO2− and ABA‐induced stomatal closing. Plant Journal 83: 567–581.

Azoulay‐Shemer T , Bagheri A , Wang C , et al. (2016) Starch biosynthesis in guard cells but not in mesophyll cells is involved in CO2‐induced stomatal closing. Plant Physiology 171: 788–798.

Azoulay‐Shemer T , Schwankl N , Rog I , Moshelion M and Schroeder JI (2018) Starch biosynthesis by AGPase, but not starch degradation by BAM1/3 and SEX1, is rate‐limiting for CO2‐regulated stomatal movements under short‐day conditions. FEBS Letters 592: 2739–2759.

Bates GW , Rosenthal DM , Sun J , et al. (2012) A comparative study of the Arabidopsis thaliana guard‐cell transcriptome and its modulation by sucrose. PLoS One 7 (11): e49641.

Brown PH and Outlaw WH (1982) Effect of fusicoccin on dark CO(2) fixation by Vicia faba guard cell protoplasts. Plant Physiology 70: 1700–1703.

Daloso DM , Antunes WC , Pinheiro DP , et al. (2015) Tobacco guard cells fix CO2 by both Rubisco and PEPcase while sucrose acts as a substrate during light‐induced stomatal opening. Plant, Cell and Environment 38: 2353–2371.

Daloso DM , Williams TCR , Antunes WC , et al. (2016) Guard cell‐specific upregulation of sucrose synthase 3 reveals that the role of sucrose in stomatal function is primarily energetic. New Phytologist 209: 1470–1483.

Dong H , Bai L , Zhang Y , et al. (2018) Modulation of guard cell turgor and drought tolerance by a peroxisomal Acetate–Malate Shunt. Molecular Plant 11: 1278–1291.

Exton JH (1988) Mechanisms of action of calcium‐mobilizing agonists: some variations on a young theme. The FASEB Journal 2: 2670–2676.

Figueroa CM and Lunn JE (2016) A tale of two sugars: trehalose 6‐phosphate and sucrose. Plant Physiology 172: 7–27.

Gago J , Douthe C , Florez‐Sarasa I , et al. (2014) Opportunities for improving leaf water use efficiency under climate change conditions. Plant Science 226: 108–119.

Gago J , de Menezes Daloso D , Figueroa CM , et al. (2016) Relationships of leaf net photosynthesis, stomatal conductance, and mesophyll conductance to primary metabolism: a multispecies meta‐analysis approach. Plant Physiology 171: 265–279.

Geigenberger P , Thormählen I , Daloso DM and Fernie AR (2017) The unprecedented versatility of the plants thioredoxin system. Trends in Plant Science 22: 249–262.

Gotow K , Taylor S and Zeiger E (1988) Photosynthetic carbon fixation in guard cell protoplasts of Vicia faba L. Plant Physiology 86: 700–705.

Hedrich R , Raschke K and Stitt M (1985) A role for fructose 2,6‐bisphosphate in regulating carbohydrate metabolism in guard cells. Plant Physiology 79: 977–982.

Hedrich R and Marten I (1993) Malate‐induced feedback regulation of plasma membrane anion channels could provide a CO2 sensor to guard cells. EMBO Journal 12: 897–901.

Horrer D , Flütsch S , Pazmino D , et al. (2016) Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening. Current Biology 26: 362–370.

Kelly G , Moshelion M , David‐Schwartz R , et al. (2013) Hexokinase mediates stomatal closure. Plant Journal 75: 977–988.

Lawson T , Oxborough K , Morison JIL and Baker NR (2002) Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO2, and humidity 1. Society 128: 52–62.

Lawson T , Simkin AJ , Kelly G and Granot D (2014) Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour. New Phytologist 203: 1064–1081.

Lu P , Outlaw WH Jr , Smith BG and Freed GA (1997) A new mechanism for the regulation of stomatal aperture size in intact leaves (accumulation of mesophyll‐derived sucrose in the guard‐cell wall of Vicia faba). Plant Physiology 114: 109–118.

McLachlan DH , Lan J , Geilfus CM , et al. (2016) The breakdown of stored triacylglycerols is required during light‐induced stomatal opening. Current Biology 26: 707–712.

Medeiros DB , Martins SCV , Cavalcanti JHF , et al. (2016) Enhanced photosynthesis and growth in atquac1 knockout mutants are due to altered organic acid accumulation and an increase in both stomatal and mesophyll conductance. Plant Physiology 170: 86–101.

Medeiros DB , Barros K , Barros JA , et al. (2017) Impaired malate and fumarate accumulation due the mutation of tonoplast dicarboxylate transporter. Plant Physiology 175 (3): 1068–1081.

Medeiros DB , Perez SL , Antunes WC , et al. (2018) Sucrose breakdown within guard cells provides substrates for glycolysis and glutamine biosynthesis during light‐induced stomatal opening. Plant Journal 94: 583–594.

Negi J , Munemasa S , Song B , et al. (2018) Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO2 and light responses in Arabidopsis guard cells. Proceedings of the National Academy of Sciences 115: 201810458.

Ng CKY and Hetherington AM (2001) Sphingolipid‐mediated signalling in plants. Annals of Botany 88: 957–965.

Ng CKY , Mcainsh MR , Gray JE , et al. (2001) Calcium‐based signalling systems in guard cells. New Phytologist 151: 109–120.

Outlaw WH , Manchester J , Dicamelli CA , et al. (1979) Photosynthetic carbon reduction pathway is absent in chloroplasts of Vicia faba guard cells. Proceedings of the National Academy of Sciences of the United States of America 76: 6371–6375.

Outlaw WH , Tarczynski MC and Anderson LC (1982) Taxonomic survey for the presence of ribulose‐1,5‐bisphosphate carboxylase activity in guard cells. Plant Physiology 70: 1218–1220.

Outlaw WHJ (2003) Integration of cellular and physiological functions of guard cells. Critical Reviews in Plant Sciences 22: 503–5229.

Pautov A , Yakovleva O , Krylova E and Gussarova G (2016) Large lipid droplets in leaf epidermis of angiosperms. Flora: Morphology, Distribution, Functional Ecology of Plants 219: 62–67.

Penfield S , Clements S , Bailey KJ , et al. (2012) Expression and manipulation of Phosphoenolpyruvate Carboxykinase 1 identifies a role for malate metabolism in stomatal closure. Plant Journal 69: 679–688.

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

Ritte G , Rosenfeld J , Rohrig K and Raschke K (1999) Rates of sugar uptake by guard cell protoplasts of Pisum sativum L. related to the solute requirement for stomatal opening. Plant Physiology 121: 647–656.

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

Sakaki T , Satoh A , Tanaka K , Omasa K and Shimazaki KI (1995) Lipids and fatty acids in guard‐cell protoplasts from Vicia faba leaves. Phytochemistry 40: 1065–1070.

Sato N (1985) Lipid biosynthesis in epidermal, guard and mesophyll cell protoplasts from leaves of Vicia faba L. Plant and Cell Physiology 26: 805–811.

Shimazaki K (1989) Ribulosebisphosphate carboxylase activity and photosynthetic O2 evolution rate in Vicia guard‐cell protoplasts. Plant Physiology 91: 459–463.

Tcherkez G , Boex‐Fontvieille E , Mahé A and Hodges M (2012) Respiratory carbon fluxes in leaves. Current Opinion in Plant Biology 15: 308–314.

Tominaga M , Kinoshita T and Shimazaki KI (2001) Guard‐cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening. Plant and Cell Physiology 42: 795–802.

Van Houtte H , Vandesteene L , Lopez‐Galvis L , et al. (2013) Overexpression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in Arabidopsis and is involved in abscisic acid‐induced stomatal closure. Plant Physiology 161: 1158–1171.

Willmer C and Fricker M (1996) Stomata. London: Chapman & Hall.

Zanella M , Borghi GL , Pirone C , et al. (2016) β‐Amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress. Journal of Experimental Botany 67: 1819–1826.

Zhai Z , Liu H , Xu C and Shanklin J (2017) Sugar potentiation of fatty acid and triacylglycerol accumulation. Plant Physiology 175 (2): 696–707.

Zhao Z , Zhang W , Stanley BA and Assmann SM (2008) Functional proteomics of arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. The Plant Cell 20: 3210–3226.

Further Reading

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

Daloso DM , Medeiros DB , dos Anjos L , et al. (2017) Metabolism within the specialized guard cells of plants. New Phytologist 216: 1018–1033.

Engineer C , Hashimoto‐sugimoto M , Negi J , et al. (2016) CO2 sensing and CO2 regulation of stomatal conductance: advances and open questions. Trends in Plant Science 21: 16–30.

Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytologist 181: 13–34.

Lima VF , Medeiros DB , Dos Anjos L , et al. (2018) Toward multifaceted roles of sucrose in the regulation of stomatal movement. Plant Signaling & Behavior 00: 1–8.

Misra BB , Acharya BR , Granot D , Assmann SM and Chen S (2015) The guard cell metabolome: functions in stomatal movement and global food security. Frontiers in Plant Science 6: 1–13.

Santelia D and Lawson T (2016) Rethinking guard cell metabolism. Plant Physiology 172: 1371–1392.

Santelia D and Lunn JE (2017) Transitory starch metabolism in guard cells: unique features for a unique function. Plant Physiology 174: 539–549.

Vavasseur A and Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytologist 165: 665–682.

Zeiger E , Talbott LD , Frechilla S , Srivastava A and Zhu J (2002) The guard cell chloroplast: a perspective for the twenty‐first century. New Phytologist 153: 415–424.

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How to Cite close
Cândido‐Sobrinho, Silvio A, Lima, Valéria F, and Daloso, Danilo M(Mar 2019) Guard Cell Metabolism. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028343]