Advertisement

Plant Molecular Biology

, Volume 98, Issue 6, pp 525–543 | Cite as

Dawn regulates guard cell proteins in Arabidopsis thaliana that function in ATP production from fatty acid beta-oxidation

  • Christoph-Martin Geilfus
  • Jue Lan
  • Sebastien Carpentier
Article

Abstract

Key message

Based on the nature of the proteins that are altered in abundance, we conclude that guard cells switch their energy source from fatty acid metabolism to chloroplast activity, at the onset of dawn.

Abstract

During stomatal opening at dawn, evidence was recently presented for a breakdown and liquidation of stored triacylglycerols in guard cells to supply ATP for use in stomatal opening. However, proteome changes that happen in the guard cells during dawn were until now poorly understood. Bad accessibility to pure and intact guard cell samples can be considered as the primary reason behind this lack of knowledge. To overcome these technical constraints, epidermal guard cell samples with ruptured pavement cells were isolated at 1 h pre-dawn, 15 min post-dawn and 1 h post-dawn from Arabidopsis thaliana. Proteomic changes were analysed by ultra-performance-liquid–chromatography-mass-spectrometry. With 994 confidently identified proteins, we present the first analysis of the A. thaliana guard cell proteome that is not influenced by side effects of guard cell protoplasting. Data are available via ProteomeXchange with identifier PXD009918. By elucidating the identities of enzymes that change in abundance by the transition from dark to light, we corroborate the hypothesis that respiratory ATP production for stomatal opening results from fatty acid beta-oxidation. Moreover, we identified many proteins that were never reported in the context of guard cell biology. Among them are proteins that might play a role in signalling or circadian rhythm.

Keywords

Guard cell Stomatal opening ATPase Beta-oxidation Triacylglycerol Dawn 

Abbreviations

ABA

Abscisic acid

LC–MS

Liquid-chromatography–mass-spectrometry

PCA

Principal component analysis

PC

Principal component

PRIDE

PRoteomics IDEntifications database

SEA

Singular enrichment analysis

SEACOMPARE

Cross comparison of SEA

DDT

Dithiothreitol

PLS

Partial least squares analysis

CSP41

Chloroplast stem-loop binding proteins

gs

Stomatal conductance

GO

Gene ontology

GC

Guard cells

DAVID

Database for annotation, visualization and integrated discovery

GAPCP

Plastidial glyceraldehyde-3-phosphate dehydrogenases

Notes

Acknowledgements

The authors are grateful to Kusay Arat for excellent technical assistance and the Coopération européenne dans le domaine de la recherche scientifique et technique is acknowledged for granting a STSM scholarship to Christoph-Martin Geilfus (Action FA1306). Dr. Deirdre McLachlan, University Bristol, is acknowledged for giving critical comments. We are grateful to Bastian Franzisky, University Hohenheim, for helping with guard cell preparation. This work was supported by the DFG research Grant GE 3111/1–1 to C.-M. Geilfus.

Author contributions

JL designed the study, grew plants and collected epidermal peels; CMG collected proteomic data; CMG and SC contributed data analysis, SC calculated statistics; CMG, SC and JL wrote the paper.

Supplementary material

11103_2018_794_MOESM1_ESM.pdf (1 mb)
Figure S1 Majority of the proteomic changes in the guard cells (GCs) are related to lipid metabolism and ATP production during dawn. Evaluation based on the 225 proteins that decreased in abundance at 1 h after dawn when compared to the sampling at 1 h before dawn. Hierarchical tree graph of overrepresented GO terms in (A) biological process-, (B) molecular function- or (C) cellular component-category. Clustering as generated by the singular enrichment analysis (SEA) tool. Boxes represent GO terms labelled by their GO ID, term definition and statistical information. The significant terms (adjusted P ≤ 0.05) are marked with colour, while non-significant terms are shown as white boxes. The degree of colour saturation of a box is positively correlated to the enrichment level of the term. Solid, dashed, and dotted lines represent two, one and zero enriched terms at both ends connected by the line (inset in (A)). The rank direction of the graph is set from left to right (PDF 1029 KB)
11103_2018_794_MOESM2_ESM.pdf (381 kb)
Supplementary material 2 (PDF 381 KB)
11103_2018_794_MOESM3_ESM.pdf (599 kb)
Supplementary material 3 (PDF 598 KB)
11103_2018_794_MOESM4_ESM.pdf (451 kb)
Figure S2 Majority of the proteomic changes in the GCs are related to carbohydrate and amino acid metabolism. Evaluation based on the 84 proteins that increased in abundance at 1 h after dawn when compared to the sampling at 1 h before dawn. Hierarchical tree graph of overrepresented GO terms in (A) biological process- or (B) molecular function-category. Clustering as generated by the singular enrichment analysis (SEA) tool. Boxes represent GO terms labelled by their GO ID, term definition and statistical information. The significant term (adjusted P ≤ 0.05) are marked with colour as described in legend of figure S1. (PDF 450 KB)
11103_2018_794_MOESM5_ESM.pdf (469 kb)
Supplementary material 5 (PDF 469 KB)
11103_2018_794_MOESM6_ESM.xlsx (132 kb)
Supplementary material 6 (XLSX 131 KB)
11103_2018_794_MOESM7_ESM.xlsx (89 kb)
Supplementary material 7 (XLSX 88 KB)
11103_2018_794_MOESM8_ESM.xlsx (47 kb)
Supplementary material 8 (XLSX 47 KB)
11103_2018_794_MOESM9_ESM.xls (128 kb)
Supplementary material 9 (XLS 128 KB)
11103_2018_794_MOESM10_ESM.xls (42 kb)
Supplementary material 10 (XLS 41 KB)
11103_2018_794_MOESM11_ESM.xls (34 kb)
Supplementary material 11 (XLS 34 KB)
11103_2018_794_MOESM12_ESM.xls (14.3 mb)
Supplementary material 12 (XLS 14658 KB)
11103_2018_794_MOESM13_ESM.xlsx (56 kb)
Supplementary material 13 (XLSX 55 KB)
11103_2018_794_MOESM14_ESM.xls (431 kb)
Supplementary material 14 (XLS 431 KB)
11103_2018_794_MOESM15_ESM.xlsx (16 kb)
Supplementary material 15 (XLSX 15 KB)
11103_2018_794_MOESM16_ESM.xlsx (11 kb)
Supplementary material 16 (XLSX 11 KB)
11103_2018_794_MOESM17_ESM.xlsx (69 kb)
Supplementary material 17 (XLSX 69 KB)

References

  1. Assmann SM, Jegla T (2016) Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. Curr Opin Plant Biol 33:157–167.  https://doi.org/10.1016/j.pbi.2016.07.003 CrossRefPubMedGoogle Scholar
  2. 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(11):e49641.  https://doi.org/10.1371/journal.pone.0049641 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-rasheid KA, 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.  https://doi.org/10.1016/j.cub.2012.11.022 CrossRefPubMedGoogle Scholar
  4. Baunsgaard L, Fuglsang AT, Jahn T, Korthout HA, De Boer AH, Palmgren MG (1998) The 14-3-3 proteins associate with the plant plasma membrane H+-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system. Plant J 13:661–671.  https://doi.org/10.1046/j.1365-313X.1998.00083.x CrossRefPubMedGoogle Scholar
  5. Buts K, Michielssens S, Hertog ML, Hayakawa E, Cordewener J, America AH, Nicolai BM, Carpentier SC (2014) Improving the identification rate of data independent label-free quantitative proteomics experiments on non-model crops: a case study on apple fruit. J Proteom 105:31–45.  https://doi.org/10.1016/j.jprot.2014.02.015 CrossRefGoogle Scholar
  6. Campos NA, Paiva LV, Panis B, Carpentier SC (2016) The proteome profile of embryogenic cell suspensions of Coffea arabica L. Proteomics 16(6):1001–1005.  https://doi.org/10.1002/pmic.201500399 CrossRefPubMedGoogle Scholar
  7. Carpentier SC, Witters E, Laukens K, Deckers P, Swennen R, Panis B (2005) Preparation of protein extracts from recalcitrant plant tissues: an evaluation of different methods for two-dimensional gel electrophoresis analysis. Proteomics.  https://doi.org/10.1002/pmic.200401222 CrossRefPubMedGoogle Scholar
  8. Carpentier SC, Panis B, Swennen R, Lammertyn J (2008) Finding the significant markers: statistical analysis of proteomic data. Methods Mol Biol 428:327–347.  https://doi.org/10.1007/978-1-59745-117-8_17 CrossRefPubMedGoogle Scholar
  9. Cornish K, Zeevaart JAD (1986) Abscisic acid accumulation by in situ and isolated guard cells of Pisum sativum L. & Vicia faba L. in relation to water stress. Plant Physiol 81:1017–1021.  https://doi.org/10.1104/pp.81.4.1017 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dodd AN, Parkinson K, Webb AA (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol 162(1):63–70.  https://doi.org/10.1111/j.1469-8137.2004.01005.x CrossRefGoogle Scholar
  11. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res.  https://doi.org/10.1093/nar/gkq310 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Flores-Tornero M, Anoman AD, Rosa-Téllez S, Toujani W, Weber AP, Eisenhut M et al (2017) Overexpression of the triose phosphate translocator (TPT) complements the abnormal metabolism and development of plastidial glycolytic glyceraldehyde-3-phosphate dehydrogenase mutants. Plant J 89(6):1146–1158.  https://doi.org/10.1111/tpj.13452 CrossRefPubMedGoogle Scholar
  13. Garagounis C, Kostaki KI, Hawkins TJ, Cummins I, Fricker MD, Hussey PJ, Hetherington AM, Sweetlove LJ (2017) Microcompartmentation of cytosolic aldolase by interaction with the actin cytoskeleton in Arabidopsis. J Exp Bot 68(5):885–898.  https://doi.org/10.1093/jxb/erx015 CrossRefPubMedGoogle Scholar
  14. Geilfus C-M (2017) The pH of the apoplast: dynamic factor with functional impact under stress. Mol Plant 10(11):1371–1386.  https://doi.org/10.1016/j.molp.2017.09.018 CrossRefPubMedGoogle Scholar
  15. Geilfus C-M, Mithöfer A, Ludwig-Müller J, Zörb C, Muehling KH (2015) Chloride-inducible transient apoplastic alkalinizations induce stomata closure by controlling abscisic acid distribution between leaf apoplast and guard cells in salt-stressed Vicia faba. New Phytol 208(3):803–816.  https://doi.org/10.1111/nph.13507 CrossRefPubMedGoogle Scholar
  16. Geilfus C-M, Carpentier SC, Zavišić A, Polle A (2017a) Changes in the fine root proteome of Fagus sylvatica L. trees associated with P-deficiency and amelioration of P-deficiency. J Proteom 169:33–40CrossRefGoogle Scholar
  17. Geilfus C-M, Tenhaken R, Carpentier SC (2017b) Transient alkalinization of the leaf apoplast stiffens the cell wall during onset of chloride-salinity in corn leaves. J. Biol Chem.  https://doi.org/10.1074/jbc.M117.799866 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Geng S, Yu B, Zhu N, Dufresne C, Chen S (2017) Metabolomics and proteomics of Brassica napus guard cells in response to low CO2. Front Mol Biosci 4:51.  https://doi.org/10.3389/fmolb.2017.00051 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Graf A, Coman D, Uhrig RG, Walsh S, Flis A, Stitt M, Gruissem W (2017) Parallel analysis of Arabidopsis circadian clock mutants reveals different scales of transcriptome and proteome regulation. Open Biol 7(3):160333.  https://doi.org/10.1098/rsob.160333 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T et al (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290(5499):2110–2113.  https://doi.org/10.1126/science.290.5499.2110 CrossRefPubMedGoogle Scholar
  21. Harwood JL (1988) Fatty acid metabolism. Annu Rev Plant Physiol Plant Mol Biol 39:101–138.  https://doi.org/10.1146/annurev.pp.39.060188.000533 CrossRefGoogle Scholar
  22. Haslam TM, Mañas-Fernández A, Zhao L, Kunst L (2012) Arabidopsis ECERIFERUM2 is a component of the fatty acid elongation machinery required for fatty acid extension to exceptional lengths. Plant Physiol 160:1164–1174.  https://doi.org/10.1104/pp.112.201640 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hedrich R, Geiger D (2017) Biology of SLAC1-type anion channels—from nutrient uptake to stomatal closure. New Phytol 216(1):46–61.  https://doi.org/10.1111/nph.14685 CrossRefPubMedGoogle Scholar
  24. Hennessey TL, Field CB (1991) Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiol 96(3):831–836.  https://doi.org/10.1104/pp.96.3.831 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908.  https://doi.org/10.1038/nature01843 CrossRefPubMedGoogle Scholar
  26. Hiyama A, Takemiya A, Munemasa S, Okuma E, Sugiyama N, Tada Y et al (2017) Blue light and CO2 signals converge to regulate light-induced stomatal opening. Nature Commun 8(1):1284.  https://doi.org/10.1038/s41467-017-01237-5 CrossRefGoogle Scholar
  27. Horrer D, Flütsch S, Pazmino D, Matthews JS, 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(3):362–370.  https://doi.org/10.1016/j.cub.2015.12.036 CrossRefPubMedGoogle Scholar
  28. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative an alysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57.  https://doi.org/10.1038/nprot.2008.211 CrossRefGoogle Scholar
  29. Inoue SI, Kinoshita T (2017) Blue light regulation of stomatal opening and the plasma membrane H+-ATPase. Plant Physiol 174(2):531–538.  https://doi.org/10.1104/pp.17.00166 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jones AM, Xuan Y, Xu M, Wang RS, Ho CH, Lalonde S et al (2014) Border control—a membrane-linked interactome of Arabidopsis. Science 344(6185):711–716.  https://doi.org/10.1126/science.1251358 CrossRefPubMedGoogle Scholar
  31. Kamata N, Okada H, Komeda Y, Takahashi T (2013) Mutations in epidermis-specific HD-ZIP IV genes affect floral organ identity in Arabidopsis thaliana. Plant J 75(3):430–440.  https://doi.org/10.1111/tpj.12211 CrossRefPubMedGoogle Scholar
  32. Kinoshita T, Shimazaki K (2002) Biochemical evidence for the requirement of 14-3-3 protein binding in activation of the guard-cell plasma membrane H+-ATPase by blue light. Plant Cell Physiol 43:1359–1365.  https://doi.org/10.1093/pcp/pcf167 CrossRefPubMedGoogle Scholar
  33. Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K (2001) Phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 414:656–660.  https://doi.org/10.1038/414656a CrossRefPubMedGoogle Scholar
  34. Kollist H, Nuhkat M, Roelfsema MRG (2014) Closing gaps: linking elements that control stomatal movement. New Phytol 203(1):44–62.  https://doi.org/10.1111/nph.12832 CrossRefPubMedGoogle Scholar
  35. Krebs M, Beyhl D, Görlich E, Al-Rasheid KAS, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci USA 107:3251–3256CrossRefPubMedGoogle Scholar
  36. Kurdyukov S, Faust A, Nawrath C, Bär S, Voisin D, Efremova N, Franke R, Schreiber L, Saedler H, Métraux JP, Yephremov A (2006) The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18(2):321–339.  https://doi.org/10.1105/tpc.105.036079 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lee MM, Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99(5):473–483.  https://doi.org/10.1016/S0092-8674(00)81536-6 CrossRefPubMedGoogle Scholar
  38. Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126(6):1109–1120.  https://doi.org/10.1016/j.cell.2006.07.034 CrossRefPubMedGoogle Scholar
  39. 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(3):596–615.  https://doi.org/10.1105/tpc.019000 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Liu J, Ji Y, Zhou J, Xing D (2016) Phosphatidylinositol 3-kinase promotes V-ATPase activation and vacuolar acidification and delays methyl jasmonate-induced leaf senescence. Plant Physiol.  https://doi.org/10.1104/pp.15.00744 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mach J (2008) Guard cell proteome reveals signals and surprises. Plant Cell 20(12):3185–3185.  https://doi.org/10.1105/tpc.108.201214 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Marín-Navarro J, Manuell AL, Wu J, Mayfield SP (2007) Chloroplast translation regulation. Photosynth Res 94:359–374.  https://doi.org/10.1007/s11120-007-9183-z CrossRefPubMedGoogle Scholar
  43. Matrosova A, Bogireddi H, Mateo-Peñas A, Hashimoto-Sugimoto M, Iba K, Schroeder JI, Israelsson-Nordström M (2015) The HT1 protein kinase is essential for red light-induced stomatal opening and genetically interacts with OST1 in red light and CO2-induced stomatal movement responses. New Phytol 208(4):1126–1137.  https://doi.org/10.1111/nph.13566 CrossRefPubMedGoogle Scholar
  44. Matsushika A, Makino S, Kojima M, Mizuno T (2000) Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell Physiol 41(9):1002–1012.  https://doi.org/10.1093/pcp/pcd043 CrossRefPubMedGoogle Scholar
  45. McLachlan DH, Lan J, Geilfus C, Dodd AN, Larson T, Baker A, Hõrak H, Kollist H, He Z, Graham I, Mickelbart MV, Hetherington AM (2016) The breakdown of stored triacylglycerols is required during light-induced stomatal opening. Curr Biol 26:1–6.  https://doi.org/10.1016/j.cub.2016.01.019 CrossRefGoogle Scholar
  46. Merilo E, Jalakas P, Laanemets K, Mohammadi O, Hõrak H, Kollist H, Brosché M (2015) Abscisic acid transport and homeostasis in the context of stomatal regulation. Mol Plant 8(9):1321–1333.  https://doi.org/10.1016/j.molp.2015.06.006 CrossRefPubMedGoogle Scholar
  47. Messinger SM, Buckley TN, Mott KA (2006) Evidence for involvement of photosynthetic processes in the stomatal response to CO2. Plant Physiol 140:771–778.  https://doi.org/10.1104/pp.105.073676 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Mi H, Muruganujan A, Thomas PD (2013) PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res.  https://doi.org/10.1093/nar/gks1118 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S et al (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion-and Ca2+-permeable channels and stomatal closure. PLoS Biol 4(10):e327.  https://doi.org/10.1371/journal.pbio.0040327 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pilot G, Lacombe B, Gaymard F, Chérel I, Boucherez J, Thibaud JB, Sentenac H (2001) Guard cell inward K+ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2. J Biol Chem 276:3215–3221.  https://doi.org/10.1074/jbc.M007303200 CrossRefPubMedGoogle Scholar
  51. Pornsiriwong W, Estavillo GM, Chan KX, Tee EE, Ganguly D, Crisp PA et al (2017) A chloroplast retrograde signal, 3′-phosphoadenosine 5′-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. ELife 6:e23361.  https://doi.org/10.7554/eLife.23361 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Pracharoenwattana I, Cornah JE, Smith SM (2005) Arabidopsis peroxisomal citrate synthase is required for fatty acid respiration and seed germination. Plant Cell 17(7):2037–2048.  https://doi.org/10.1105/tpc.105.031856 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Qi Y, Armbruster U, Schmitz-Linneweber C, Delannoy E, De Longevialle AF, Rühle T, Small I, Jahns P, Leister D (2012) Arabidopsis CSP41 proteins form multimeric complexes that bind and stabilize distinct plastid transcripts. J Exp Bot 63:1251–1270.  https://doi.org/10.1093/jxb/err347 CrossRefPubMedGoogle Scholar
  54. Roelfsema MRG, Hedrich R (2002) Studying guard cells in the intact plant: modulation of stomatal movement by apoplastic factors. New Phytol 153(3):425–431.  https://doi.org/10.1046/j.0028-646X.2001 CrossRefGoogle Scholar
  55. Roelfsema M, Hanstein S, Felle H, Hedrich R (2002) CO2 provides an intermediate link in the red light response of guard cells. Plant J 32:65–75.  https://doi.org/10.1046/j.1365-313X.2002.01403.x CrossRefPubMedGoogle Scholar
  56. Santelia D, Lunn JE (2017) Transitory starch metabolism in guard cells: unique features for a unique function. Plant Physiol 174(2):539–549.  https://doi.org/10.1104/pp.17.00211 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Schäfer N, Maierhofer T, Herrmann J, Jørgensen ME, Lind C, von Meyer K et al (2018) A tandem amino acid residue motif in guard cell SLAC1 anion channel of grasses allows for the control of stomatal aperture by nitrate. Curr Biol 28(9):1370–1379CrossRefPubMedGoogle Scholar
  58. Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–1229.  https://doi.org/10.1016/S0092-8674(00)81465-8 CrossRefPubMedGoogle Scholar
  59. Shimakata T, Stumpf PK (1982) Isolation and function of spinach leaf β-ketoacyl-[acyl-carrier-protein] synthases. Proc Natl Acad Sci 79:5808–5812.  https://doi.org/10.1073/pnas.79.19.5808 CrossRefPubMedGoogle Scholar
  60. Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247.  https://doi.org/10.1146/annurev.arplant.57.032905.105434 CrossRefPubMedGoogle Scholar
  61. Somers DE, Webb AA, Pearson M, Kay SA (1998) The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125(3):485–494PubMedGoogle Scholar
  62. Stern DB, Gruissem W (1987) Control of plastid gene expression: 3′ inverted repeats act as mRNA processing and stabilizing elements, but do not terminate transcription. Cell 51:1145–1157.  https://doi.org/10.1016/0092-8674(87)90600-3 CrossRefPubMedGoogle Scholar
  63. Taiz L, Zeiger E, Møller I, Murphy A (2015) In: Plant physiology and development, 6th edn. Sinauer Associates, SunderlandGoogle Scholar
  64. Takemiya A, Sugiyama N, Fujimoto H, Tsutsumi T, Yamauchi S, Hiyama A, Tada Y, Christie JM, Shimazaki K (2013) Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening. Nat Commun.  https://doi.org/10.1038/ncomms3094 CrossRefPubMedGoogle Scholar
  65. Tominaga R, Iwata M, Okada K, Wada T (2007) Functional analysis of the epidermal-specific MYB genes CAPRICE and WEREWOLF in Arabidopsis. Plant Cell 19(7):2264–2277.  https://doi.org/10.1105/tpc.106.045732 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Ullah H, Scappini EL, Moon AF, Williams LV, Armstrong DL, Pedersen LC (2008) Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana. Protein Sci 17(10):1771–1780.  https://doi.org/10.1110/ps.035121.108 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277(5329):1113–1116.  https://doi.org/10.1126/science.277.5329.1113 CrossRefPubMedGoogle Scholar
  68. Wang ZY, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93:1207–1217.  https://doi.org/10.1016/S0092-8674(00)81464-6 CrossRefPubMedGoogle Scholar
  69. Wang Z, Wang F, Hong Y, Huang J, Shi H, Zhu JK (2016) Two chloroplast proteins suppress drought resistance by affecting ROS production in guard cells. Plant Physiol 172(4):2491–2503.  https://doi.org/10.1104/pp.16.00889 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Wang W, Liu Z, Bao LJ, Zhang SS, Zhang CG, Li X et al (2017) The Rho-GTPase RopGEF2-ROP7/ROP2 pathway activated by phyB suppresses red light-induced stomatal opening. Plant Physiol 174(2):717–731.  https://doi.org/10.1104/pp.16.01727 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Yamauchi S, Takemiya A, Sakamoto T, Kurata T, Tsutsumi T, Kinoshita T, Shimazaki K (2016) The plasma membrane H+-ATPase AHA1 plays a major role in stomatal opening in response to blue light. Plant Physiol 171:2731–2743.  https://doi.org/10.1104/pp.16.01581 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Yang J, Stern DB (1997) The spinach chloroplast endoribonuclease CSP41 cleaves the 3′-untranslated region of petD mRNA primarily within its terminal stem-loop structure. J Biol Chem 272:12874–12880.  https://doi.org/10.1074/jbc.272.19.12874 CrossRefPubMedGoogle Scholar
  73. Yang J, Schuster G, Stern DB (1996) CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. Plant Cell 8:1409–1420.  https://doi.org/10.1105/tpc.8.8.1409 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Zeeman SC, Delatte T, Messerli G, Umhang M, Stettler M, Mettler-Altmann T, Streb S, Reinhold H, Kötting O (2007) Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms. Funct Plant Biol 34(6):465–473CrossRefGoogle Scholar
  75. Zeiger E, Zhu J (1998) Role of zeaxanthin in blue light photoreception and the modulation of light-CO2 interactions in guard cells. J Exp Bot 498(1):433–442.  https://doi.org/10.1093/jxb/49 CrossRefGoogle Scholar
  76. Zhang XF, Jiang T, Wu Z, Du SY, Yu YT, Jiang SC, Lu K, Feng XJ, Wang XF, Zhang DP (2013) Cochaperonin CPN20 negatively regulates abscisic acid signaling in Arabidopsis. Plant Mol Biol 83(3):205–218.  https://doi.org/10.1007/s11103-013-0082-8 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zhao Z, Zhang W, Stanley BA, Assmann SM (2008) Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell 20:3210–3226.  https://doi.org/10.1105/tpc.108.063263 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Division of Controlled Environment Horticulture, Faculty of Life Sciences, Albrecht Daniel Thaer-Institute of Agricultural and Horticultural SciencesHumboldt-University of BerlinBerlinGermany
  2. 2.Proteomics Core FacilitySYBIOMA, KU LeuvenLeuvenBelgium
  3. 3.School of Biological SciencesUniversity of BristolBristolUK
  4. 4.Division of Crop Biotechnics, Department of BiosystemsKU LeuvenLeuvenBelgium

Personalised recommendations