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Trees

, Volume 33, Issue 6, pp 1679–1693 | Cite as

How do coffee trees deal with severe natural droughts? An analysis of hydraulic, diffusive and biochemical components at the leaf level

  • Samuel C. V. Martins
  • Matheus L. Sanglard
  • Leandro E. Morais
  • Paulo E. Menezes-Silva
  • Rafael Mauri
  • Rodrigo T. Avila
  • Camilo E. Vital
  • Amanda A. Cardoso
  • Fábio M. DaMattaEmail author
Original Article

Abstract

Key message

We analysed field-grown coffee trees that faced the most severe drought event in the last 28 years in Brazil. Vulnerability curves indicated that water potentials were low enough to decrease leaf hydraulic conductance and carbohydrate content under drought. However, individual tree mortality was not observed indicating a great resilience of coffee to drought stress.

Abstract

Drought affects leaf photosynthesis by acting on hydraulic, diffusive and/or biochemical components. Here, we analysed two field-grown coffee (Coffea arabica L.) cultivars (Catuaí and Catimor) subjected to a severe natural drought (the most severe drought event in the last 28 years in Brazil) followed by a subsequent rehydration. We estimated leaf hydraulic vulnerability and found that the leaf water potential under drought reached values that were low enough to cause drastic decreases (up to 90%) in leaf hydraulic conductance (Kleaf) in both cultivars. Such Kleaf loss was associated with a reduced stomatal conductance (gs) under drought (c. 70%) and likely limited gas-exchange recovery upon rainfall as abscisic acid levels and gs were not correlated. Net photosynthesis rates (An) were largely limited by diffusive constraints, with gs explaining c. 90% of the variation in An. Rubisco carboxylation capacity and soluble protein content remained unaltered, in contrast to starch content which was drastically reduced by drought. Soluble sugars were less affected, with hexoses having an apparent role as osmolytes. Even though hydraulics, gas-exchange traits and non-structural carbohydrate pools were negatively affected, coffee trees did not present individual mortality, demonstrating a great resilience to drought events.

Keywords

Leaf hydraulics Hydraulic vulnerability Coffea arabica Stomatal control Abscisic acid 

Notes

Acknowledgements

This research was supported by the National Council for Scientific and Technological Development (CNPq, Brazil) through research funding granted to FMD. We are grateful for the scholarships that were granted by the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES), the Foundation for Research Assistance of Minas Gerais State, Brazil (FAPEMIG) and CNPq. We are also thankful to the Núcleo de Análises de Biomoléculas (NUBIOMOL) for providing the facilities to perform the ABA analysis and to Professor Dimas Mendes Ribeiro for the clever insights regarding alternative ABA roles in leaf development.

Supplementary material

468_2019_1889_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1178 kb)

References

  1. Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci USA 109:233–237CrossRefPubMedGoogle Scholar
  2. Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B, Jansen S (2016) Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc Natl Acad Sci USA 113:5024–5029CrossRefPubMedGoogle Scholar
  3. Araújo WL, Dias PC, Moraes GABK, Celin EF, Cunha RL, Barros RS, DaMatta FM (2008) Limitations to photosynthesis in coffee leaves from different canopy positions. Plant Physiol Biochem 46:884–890CrossRefPubMedGoogle Scholar
  4. Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation—an alternative respiratory substrate for stressed plants. Trends Plant Sci 16:489–498PubMedGoogle Scholar
  5. Bartlett M, Klein T, Jansen S, Choat B, Sack L (2016) The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc Natl Acad Sci USA 113:13098–13103CrossRefPubMedGoogle Scholar
  6. Batista KD, Araújo WL, Antunes WC, Cavatte PC, Moraes GABK, Martins SCV, DaMatta FM (2012) Photosynthetic limitations in coffee plants are chiefly governed by diffusive factors. Trees 26:459–468CrossRefGoogle Scholar
  7. Blackman CJ, Brodribb TJ (2011) Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Funct Plant Biol 38:118–126CrossRefGoogle Scholar
  8. Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123CrossRefPubMedGoogle Scholar
  9. Bouche PS, Delzon S, Choat B, Badel E, Brodribb TJ, Burlett R, Cochard H, Charra-Vaskou K, Lavigne B, Li S et al (2016) Are needles of Pinus pinaster more vulnerable to xylem embolism than branches? New insights from X-ray computed tomography. Plant Cell Environ 39:860–870CrossRefPubMedGoogle Scholar
  10. Brodribb TJ, Cochard H (2009) hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584CrossRefPubMedPubMedCentralGoogle Scholar
  11. Brodribb TJ, Holbrook NM, Edwards EJ, Gutierrez MV (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450CrossRefGoogle Scholar
  12. Bunce JA (1990) Abscisic acid mimics effects of dehydration on area expansion and photosynthetic partitioning in young soybean leaves. Plant Cell Environ 13:295–298CrossRefGoogle Scholar
  13. Bunn C, Läderach P, Ovalle OO, Kirschke D (2015) A bitter cup: climate change profile of global production of Arabica and Robusta coffee. Clim Change 129:89–101CrossRefGoogle Scholar
  14. Chaves ARM, Martins SCV, Batista KD, Celin EF, DaMatta FM (2012) Varying leaf-to-fruit ratios affect branch growth and dieback, with little to no effect on photosynthesis, carbohydrate or mineral pools, in different canopy positions of field-grown coffee trees. Environ Exp Bot 77:207–218CrossRefGoogle Scholar
  15. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–756CrossRefPubMedGoogle Scholar
  16. Cochard H, Badel E, Herbette S, Delzon S, Choat B, Jansen S (2013) Methods for measuring plant vulnerability to cavitation: a critical review. J Exp Bot 64:4779–4791CrossRefPubMedGoogle Scholar
  17. Cooil BJ, Nakayama M (1953) Carbohydrate balance as a major factor affecting yield of the coffee tree. Hawaii Agric Exp Station Prog Notes 91:1–16Google Scholar
  18. DaMatta FM, Maestri M, Barros RS (1997) Photosynthetic performance of two coffee species under drought. Photosynthetica 34:257–264CrossRefGoogle Scholar
  19. DaMatta FM, Chaves ARM, Pinheiro HA, Ducatti C, Loureiro ME (2003) Drought tolerance of two field-grown clones of Coffea canephora. Plant Sci 164:111–117CrossRefGoogle Scholar
  20. DaMatta FM, Ronchi CP, Maestri M, Barros RS (2007) Ecophysiology of coffee growth and production. Braz J Plant Physiol 19:485–510CrossRefGoogle Scholar
  21. DaMatta FM, Grandis A, Arenque BC, Buckeridge MS (2010a) Impacts of climate changes on crop physiology and food quality. Food Res Int 43:1814–1823CrossRefGoogle Scholar
  22. DaMatta FM, Ronchi CP, Maestri M, Barros RS (2010b) Coffee: environment and crop physiology. In: DaMatta FM (ed) Ecophysiology of tropical tree crops. Nova Science Publishers, New York, pp 181–216Google Scholar
  23. DaMatta FM, Godoy AG, Menezes-Silva PE, Martins SCV, Sanglard LMVP, Morais LE, Torre-Neto A, Ghini R (2016) Sustained enhancement of photosynthesis in coffee trees grown under free-air CO2 enrichment conditions: disentangling the contributions of stomatal, mesophyll, and biochemical limitations. J Exp Bot 67:341–352CrossRefPubMedGoogle Scholar
  24. DaMatta FM, Avila RT, Cardoso AA, Martins SCV, Ramalho JC (2018) Physiological and agronomic performance of the coffee crop in the context of climate change and global warming: a review. J Agric Food Chem 66:5264–5274CrossRefPubMedGoogle Scholar
  25. Dias PC, Araujo WL, Moraes GABK, Barros RS, DaMatta FM (2007) Morphological and physiological responses of two coffee progenies to soil water availability. J Plant Physiol 164:1639–1647CrossRefPubMedGoogle Scholar
  26. Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687CrossRefPubMedGoogle Scholar
  27. Ewers FW, Cochard H, Tyree MT (1997) A survey of root pressures in vines of a tropical lowland forest. Oecologia 110:191–196CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ewers FW, Améglio T, Cochard H, Beaujard F, Martignac M, Vandame M, Bodet C, Cruiziat P (2001) Seasonal variation in xylem pressure of walnut trees: root and stem pressures. Tree Physiol 21:1123–1132CrossRefPubMedGoogle Scholar
  29. Flexas J, Scoffoni C, Gago J, Sack L (2013) Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. J Exp Bot 64:3965–3981CrossRefPubMedGoogle Scholar
  30. Galvez DA, Landhausser SM, Tyree MT (2011) Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol 31:250–257CrossRefPubMedGoogle Scholar
  31. Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 990:87–92CrossRefGoogle Scholar
  32. Hartmann H, Ziegler W, Kolle O, Trumbore S (2013) Thirst beats hunger—declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200:340–349CrossRefPubMedGoogle Scholar
  33. Hernandez-Santana V, Rodriguez-Dominguez CM, Fernández JE, Diaz-Espejo A (2016) Role of leaf hydraulic conductance in the regulation of stomatal conductance in almond and olive in response to water stress. Tree Physiol 36:725–735CrossRefPubMedGoogle Scholar
  34. Hochberg U, Herrera JC, Cochard H, Badel E (2016) Short-time xylem relaxation results in reliable quantification of embolism in grapevine petioles and sheds new light on their hydraulic strategy. Tree Physiol 36:748–755CrossRefPubMedGoogle Scholar
  35. Hochberg U, Windt CW, Ponomarenko A, Zhang YJ, Gersony J, Rockwell FE, Holbrook NM (2017) Stomatal closure, basal leaf embolism and shed- ding protect the hydraulic integrity of grape stems. Plant Physiol 174:764–775CrossRefPubMedPubMedCentralGoogle Scholar
  36. ICO (International Coffee Organization) (2014) World coffee trade (1963–2013): a review of the markets, challenges and opportunities facing the sector. ICC (International Coffee Council), 111-5 Rev. 1, p 29. http://www.ico.org/show_news.asp?id=361. Accessed 20 May 2015
  37. Johnson DM, Wortemann R, McCulloh KA, Jordan-Meille L, Ward E, Warren JM, Palmroth S, Domec JC (2016) A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species. Tree Physiol 36:983–993CrossRefPubMedGoogle Scholar
  38. Klepsch M, Zhang Y, Kotowska MM, Lamarque LJ, Nolf M, Schuldt B, Torres-Ruiz JM, Qin D-W, Choat B, Delzon S, Scoffoni C, Cao K, Jansen S (2018) Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy. J Exp Bot Bot 69:5611–5623Google Scholar
  39. Lima ALS, DaMatta FM, Pinheiro HA, Totola MR, Loureiro ME (2002) Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit conditions. Environ Exp Bot 47:239–247CrossRefGoogle Scholar
  40. Losso A, Bär A, Dämon B, Dullin C, Ganthaler A, Petruzellis F, Savi T, Tromba G, Nardini A, Mayr S, Beikircher B (2018) Insights from in vivo micro-CT analysis: testing the hydraulic vulnerability segmentation in Acer pseudoplatanus and Fagus sylvatica seedlings. New Phytol 221:1831–1842CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lovisolo C, Perrone I, Hartung W, Schubert A (2008) An abscisic acid-related reduced transpiration promotes gradual embolism repair when grapevines are rehydrated after drought. New Phytol 180:642–651CrossRefPubMedGoogle Scholar
  42. Lu Y, Alejandra Equiza M, Deng X, Tyree MT (2010) Recovery of Populus tremuloides seedlings following severe drought causing total leaf mortality and extreme stem embolism. Physiol Plant 140:246–257PubMedGoogle Scholar
  43. Manzoni S, Vico G, Katul G, Palmroth S, Jackson RB, Porporato A (2013) Hydraulic limits on maximum plant transpiration and the emergence of the safety-efficiency trade-off. New Phytol 198:169–178CrossRefPubMedGoogle Scholar
  44. Marraccini P, Vinecky F, Alves GSC, Ramos HJO, Elbelt S, Vieira NG, Carneiro FA, Sujii PS, Alekcevetch JC, Silva VA, DaMatta FM, Ferrão MAG, Leroy T, Pot D, Vieira LGE, Silva FR, Andrade AC (2012) Differentially expressed genes and proteins upon drought acclimation in tolerant and sensitive genotypes of Coffea canephora. J Exp Bot 63:4191–4212CrossRefPubMedPubMedCentralGoogle Scholar
  45. Martins SCV, Galmés JG, Molins A, DaMatta FM (2013) Improving the estimation of mesophyll conductance: on the role of electron transport rate correction and respiration. J Exp Bot 64:3285–3298CrossRefPubMedPubMedCentralGoogle Scholar
  46. Martins SCV, Galmés JG, Cavatte PC, Pereira LF, Ventrella MC, Damatta FM (2014) Understanding the low photosynthetic rates of sun and shade coffee leaves: bridging the gap on the relative roles of hydraulic, diffusive and biochemical constraints to photosynthesis. PLoS One 9:e95571CrossRefPubMedPubMedCentralGoogle Scholar
  47. Martin-StPaul NK, Longepierre D, Huc R, Delzon S, Burlett R, Joffre R, Rambal S, Cochard H (2014) How reliable are methods to assess xylem vulnerability to cavitation? The issue of “open vessel” artifact in oaks. Tree Physiol 34:894–905CrossRefPubMedGoogle Scholar
  48. McAdam SAM, Brodribb TJ (2015) The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiol 167:833–843CrossRefPubMedPubMedCentralGoogle Scholar
  49. McAdam SAM, Brodribb TJ (2016) Linking turgor with ABA biosynthesis: implications for stomatal responses to vapor pressure deficit across land plants. Plant Physiol 171:2008–2016CrossRefPubMedPubMedCentralGoogle Scholar
  50. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739CrossRefPubMedGoogle Scholar
  51. Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37CrossRefPubMedPubMedCentralGoogle Scholar
  52. Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–216CrossRefGoogle Scholar
  53. Nardini A, Luglio J (2014) Leaf hydraulic capacity and drought vulnerability: possible trade-offs and correlations with climate across three major biomes. Funct Ecol 28:810–818CrossRefGoogle Scholar
  54. Nardini A, Ounapuu-Pikas E, Savi T (2014) When smaller is better: leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes. Funct Plant Biol 41:972–982CrossRefGoogle Scholar
  55. Patel RZA (1970) Note on the seasonal variations in starch content of different parts of Arabica coffee trees. East Afr Agric For J 36:1–4CrossRefGoogle Scholar
  56. Pereira L, Bittencourt PRL, Oliveira RS, Junior MBM, Barros FV, Ribeiro RV, Mazzafera P (2016) Plant pneumatics: stem air flow is related to embolism—new perspectives on methods in plant hydraulics. New Phytol 211:357–370CrossRefPubMedGoogle Scholar
  57. Pinheiro HA, DaMatta FM, Chaves ARM, Fontes EPB, Loureiro ME (2004) Drought tolerance in relation to protection against oxidative stress in clones of Coffea canephora subjected to long-term drought. Plant Sci 167:1307–1314CrossRefGoogle Scholar
  58. Pinheiro HA, DaMatta FM, Chaves ARM, Loureiro ME, Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. Ann Bot 96:101–108CrossRefPubMedPubMedCentralGoogle Scholar
  59. Praxedes SC, DaMatta FM, Loureiro ME, Ferrão MAG, Cordeiro AT (2006) Effects of long-term soil drought on photosynthesis and carbohydrate metabolism in mature robusta coffee (Coffea canephora Pierre var. kouillou) leaves. Environ Exp Bot 56:263–273CrossRefGoogle Scholar
  60. Puri E, Hoch G, Körner C (2015) Defoliation reduces growth but not carbon reserves in Mediterranean Pinus pinaster trees. Trees 29:1187–1196CrossRefGoogle Scholar
  61. Quentin AG, Pinkard EA, Ryan MG, Tissue DT, Baggett LS, Adams HD, Maillard P, Marchand J, Landhäusser SM, Lacointe A et al (2015) Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol 35:1146–1165PubMedGoogle Scholar
  62. Rodrigues WP, Machado-Filho JA, Silva JR, Figueiredo FAMMA, Ferraz TM, Ferreira LS, Bezerra LBS, Abreu DP, Bernado WP, Passos LC, Sousa EF, Glenn DM, Ramalho JC, Campostrini E (2016) Whole-canopy gas exchanges in Coffea sp. is affected by supra-optimal temperature and light distribution within the canopy: the insights from an improved multi-chamber system. Sci Hortic 211:194–202CrossRefGoogle Scholar
  63. Rodriguez-Dominguez CM, Carins Murphy MR, Lucani C, Brodribb TJ (2018) Mapping xylem failure in disparate organs of whole plants reveals extreme resistance in olive roots. New Phytol 218:1025–1035CrossRefPubMedGoogle Scholar
  64. Ronchi CP, DaMatta FM, Batista KD, Moraes GABK, Loureiro ME, Ducatti C (2006) Growth and photosynthetic downregulation in Coffea arabica in response to restricting root volume. Funct Plant Biol 33:1013–1023CrossRefGoogle Scholar
  65. Scoffoni C, Sack L (2015) Are leaves “freewheelin”? Testing for a Wheeler-type effect in leaf xylem hydraulic decline. Plant Cell Environ 38:534–543CrossRefPubMedGoogle Scholar
  66. Scoffoni C, Albuquerque C, Brodersen CR, Townes SV, John GP, Bartlett MK, Buckley TN, McElrone AJ, Sack L (2017) Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiol 173:1197–1210CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sevanto S, Mcdowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ 37:153–161CrossRefPubMedGoogle Scholar
  68. Silva EA, DaMatta FM, Ducatti C, Regazzi AJ, Barros RS (2004) Seasonal changes in vegetative growth and photosynthesis of Arabica coffee trees. Field Crops Research 89:349–357CrossRefGoogle Scholar
  69. Silva PEM, Cavatte PC, Morais LE, Medina EF, DaMatta FM (2013) The functional divergence of biomass partitioning, carbon gain and water use in Coffea canephora in response to the water supply: implications for breeding aimed at improving drought tolerance. Environ Exp Bot 87:49–57CrossRefGoogle Scholar
  70. Skelton RP, Brodribb TJ, Choat B (2017a) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol 214:561–569CrossRefPubMedGoogle Scholar
  71. Skelton RP, Brodribb TJ, McAdam SAM, Mitchell PJ (2017b) Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance: evidence from an evergreen woodland. New Phytol 215:1399–1412CrossRefPubMedGoogle Scholar
  72. Skelton RP, Dawson TE, Thompson SE, Shen Y, Weitz AP, Ackerly D (2018) Low Vulnerability to xylem embolism in leaves and stems of north American Oaks. Plant Physiol 177:1066–1077CrossRefPubMedPubMedCentralGoogle Scholar
  73. Tausend PC, Goldstein G, Meinzer FC (2000) Water utilization, plant hydraulic properties and xylem vulnerability in three contrasting coffee (Coffea arabica) cultivars. Tree Physiol 20:159–168CrossRefPubMedGoogle Scholar
  74. Tyree MT, Cochard H, Cruiziat P, Sinclair B, Ameglio T (1993) Drought-induced leaf shedding in walnut: evidence for vulnerability segmentation. Plant Cell Environ 16:879–882CrossRefGoogle Scholar
  75. Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: is there a trade-off to hydraulic efficiency for vulnerability to dysfunction? Int Assoc Wood Anat 15:335–360Google Scholar
  76. Urli M, Porté AJ, Cochard H, Guengant Y, Burlett R, Delzon S (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33:672–683CrossRefPubMedGoogle Scholar
  77. Wason JW, Anstreicher KS, Stephansky N, Huggett BA, Brodersen CR (2018) Hydraulic safety margins and air-seeding thresholds in roots, trunks, branches and petioles of four northern hardwood trees. New Phytol 219:77–88CrossRefPubMedGoogle Scholar
  78. Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environ 36:1938–1949PubMedGoogle Scholar
  79. Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wilson KB, Baldocchi DD, Hanson PJ (2000) Quantifying stomatal and non-stomatal limitations to carbon assimilation resulting from leaf aging and drought in mature deciduous tree species. Tree Physiol 20:787–797CrossRefPubMedGoogle Scholar
  81. Zargar A, Sadiq R, Naser B, Khan FI (2011) A review of drought indices. Environ Rev 19:333–349CrossRefGoogle Scholar
  82. Zhang SQ, Outlaw WH (2001) Abscisic acid introduced into the transpiration stream accumulates in the guard-cell apoplast and causes stomatal closure. Plant Cell Environ 24:1045–1054CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Samuel C. V. Martins
    • 1
  • Matheus L. Sanglard
    • 1
  • Leandro E. Morais
    • 1
  • Paulo E. Menezes-Silva
    • 1
  • Rafael Mauri
    • 1
  • Rodrigo T. Avila
    • 1
  • Camilo E. Vital
    • 2
  • Amanda A. Cardoso
    • 1
  • Fábio M. DaMatta
    • 1
    Email author
  1. 1.Departamento de Biologia VegetalUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Núcleo de BiomoléculasUniversidade Federal de ViçosaViçosaBrazil

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