Leaf phytohormone levels and stomatal control in an evergreen woody species under semiarid environment in a Brazilian seasonally dry tropical forest
Tóm tắt
Phytohormones are essential for controlling abilities of plant species to overcome stress conditions, and influence some aspects of stomatal control, preventing excessive water loss. This study investigates the correlation between foliar phytohormones levels, water status and stomatal conductance in an evergreen woody species (Cynophalla flexuosa) throughout dry and rainy seasons, and the transition between them. We measured stomatal conductance (gs), xylem branch water potential (Ѱx), and leaf concentration of abscisic acid (ABA), jasmonic acid (JA), salicylic acid (SA) and trans-zeatin (tZ). Stomatal conductance was more sensitive to atmospheric conditions, such as VPD than to soil water balance. However, we found correlation between gs and Ѱx, suggesting that these direct water availability measures were a good proxy to explain gs in C. flexuosa. Moreover, ABA leaf concentration had no effect on gs, but ABA and tZ interaction was important to the phenological behaviour of this species. Cytokinins act in delaying leaf senescence, which is crucial to evergreen species, and it is opposite to ABA’s action. JA also showed a significant interaction to ABA, and kept high foliar level during wet season. ABA levels varied throughout the year, and its concentration itself was less important to gs than the interaction to other phytohormones, such as tZ and JA. In conclusion, although ABA did not directly affect stomatal conductance in C. flexuosa, the interaction between ABA, tZ and JA likely played a role in the regulation of stomatal behavior in this species.
Tài liệu tham khảo
Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131. https://doi.org/10.1093/jxb/ern251
Albacete A, Martinez-Andujar C, Ghanem ME, Acosta M, Sanchez- Bravo J, Asins MJ, Cuartero J, Lutts S, Dodd IC, Perez-Alfocea F (2009) Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato. Plant Cell Environ 32:928–938. https://doi.org/10.1111/j.1365-3040.2009.01973.x
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Barkosky RR, Einhellig FA (1993) Effects of salicyclic acid on plant water relationship. J Chem Ecol 19:237–247. https://doi.org/10.1007/BF00993692
Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-Rasheid KAS, Sonnewald S, Sonnewald U, Kneitz S, Lachmann N, Mendel RR, Bittner F, Hetheringhton AM, Hedrich R (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
Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585. https://doi.org/10.1126/science.1197985
Daszkowska-Golec A, Szarejko I (2013) Open or close the gate – stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138–154. https://doi.org/10.3389/fpls.2013.00138
Diego ND, Pérez-Alfocea F, Cantero E, Lacuesta M, Moncaleán P (2012) Physiological response to drought in radiata pine: phytohormone implication at leaf level. Tree Physiol 32:435–449. https://doi.org/10.1093/treephys/tps029
Dobrev PI, Kaminek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr 950:21–29
Escandón M, Cañal MJ, Pascual J, Pinto G, Correia B, Amaral J, Meijón M (2016) Integrated physiological and hormonal profile of heat-induced thermotolerance in Pinus radiata. Tree Physiol 36:63–77. https://doi.org/10.1093/treephys/tpv127
Falcão H, Medeiros CDB, Silva BLR, Sampaio EVSB., Almeida-Cortez J, Santos MG (2015) Phenotypic plasticity and ecophysiological strategies in a tropical dry forest chronosequence: a study case with Poincianella pyramidalis. For Ecol Manage 340:62–69. https://doi.org/10.1016/j.foreco.2014.12.029
Falcão HM, Medeiros CD, Almeida-Cortez J, Santos MG (2017) Leaf construction cost is related to water availability in three species of different growth forms in a Brazilian tropical dry forest. Theor Exp Plant Physiol 29:95–108. https://doi.org/10.1007/s40626-017-0087-9
Figueiredo KV, Oliveira MT, Arruda ECP, Silva BCF, Santos MG (2015) Changes in leaf epicuticular wax, gas exchange and biochemistry metabolism between Jatropha mollissima and Jatropha curcas under semi-arid conditions. Acta Physiol Plant 37:2–11. https://doi.org/10.1007/s11738-015-1855-2
Frosi G, Oliveira MT, Almeida-Cortez J, Santos MG (2013) Ecophysiological performance of Calotropis procera: an exotic and evergreen species in Caatinga, Brazilian semi-arid. Acta Physiol Plant 35:335–344. https://doi.org/10.1007/s11738-012-1076-x
Fuchs EE, Livingston NJ (1996) Hydraulic control of stomatal conductance in Douglas fir [Pseudotsuga menzlesii (M’trb.) Franco] and alder [AInus rubra (Bong)] seedlings. Plant Cell Environ 19:1091–1098. https://doi.org/10.1111/j.1365-3040.1996.tb00216.x
Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Env Exp Bot 68:14–25. https://doi.org/10.1016/j.envexpbot.2009.08.005
IPA (2015) Instituto Agronômico de Pernambuco.Sessão de Índices Pluviométricos. http://www.ipa.br/indice_pluv.php#calendario_indices. Accessed 7 July 2015
Lebrija-Trejos E, Pérez-García EA, Meave JA, Poorter L (2011) Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:477–489. https://doi.org/10.1017/S0266467411000253
Lima ALA, Sampaio EVSB., Castro CC, Rodal MJN, Antonino ACD, Melo AL (2012) Do the phenology and functional stem attributes of woody species allow for the identification of functional groups in the semiarid region of Brazil? Trees 26:1605–1616. https://doi.org/10.1007/s00468-012-0735-2
McAdam SA, Brodribb TJ (2016) Linking turgor with ABA biosynthesis: implications for stomatal responses to vapor pressure deficit across land plants. Plant Physiol 171:2008–2016. https://doi.org/10.1104/pp.16.00380
McGarigal K, Cushman SA, Stafford S (2000) Multivariate statistics for wildlife ecology research. Springer, New York
Miles L, Newton A, DeFries RS, Ravilious C, May I, Blyth S, Kapos V, Gordon JE (2006) A global overview of the conservation status of tropical dry forests. J Biogeogr 33:491–502. https://doi.org/10.1111/j.1365-2699.2005.01424.x
Morales M, Garcia QS, Munné-Bosch S (2015) Ecophysiological response to seasonal variations in water availability in the arborescent, endemic plant Vellozia gigantea. Tree Physiol 35:253–265. https://doi.org/10.1093/treephys/tpv012
Mott KA, Peak D (2013) Testing a vapour-phase model of stomatal responses to humidity. Plant Cell Environ 36:936–944. https://doi.org/10.1111/pce.12026
Noir S, Bömer M, Takahashi N, Ishida T, Tsui TL, Balbi V, Shanahan H, Sugimoto K, Devoto A (2013) Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 161:1930–1951. https://doi.org/10.1104/pp.113.214908
Oliveira MT, Matzek V, Medeiros CDB, Costa RR, Falcão HM, Santos MG (2014) Stress tolerance and ecophysiological ability of an invader and a native species in a seasonally dry tropical forest. PLoS ONE 9:1–11. https://doi.org/10.1371/journal.pone.0105514
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295. https://doi.org/10.1016/j.pbi.2011.02.001
Pospisilova J (2003) Participation of phytohormones in the stomatal regulation of gas exchange during water stress. Biol Plant 46:491–506. https://doi.org/10.1023/A:1024894923865
Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636. https://doi.org/10.1073/pnas.0709453104
Rivero RM, Gimeno J, Deynze AV, Walia H, Blumwald E (2010) Enhanced cytokinin synthesis in tobacco plants expressing PSARK:IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol 51:1929–1941. https://doi.org/10.1093/pcp/pcq143
Rolim GS, Sentelhas PC, Barbieri V (1998) Planilhas no ambiente Excel™ para os cálculos de balanços hídricos:normal, sequencial, de cultura e de produtividade real e potencial. Ver Bras Agromet 6:133–137
Santana DG, Ranal MA (2006) Linear correlation in experimental design models applied to seed germination. Seed Sci Technol 34:233–239. https://doi.org/10.15258/sst.2006.34.1.28
Santos MG, Oliveira MT, Figueiredo KV, Falcão HM, Arruda ECP, Almeida-Cortez J, Sampaio EVSB., Ometto JPHB., Menezes RSC, Oliveira AFM, Pompelli MF, Antonino ACD (2014) Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes? Theor Exp Plant Physiol 26:83–99. https://doi.org/10.1007/s40626-014-0008-0
Scholander PF, Hammel HT, Hemmingsen EA, Bradstreet ED (1964) Hydrostatic pressure and osmotic potentials in leaves of mangroves and some other plants. Proc Natl Acad Sci USA 51:119–125
Shepherd GJ (2010) Fitopac 2.1.2.85. Manual do Usuário. Universidade Estadual de Campinas, Campinas
Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Grow Regul 39:137–141. https://doi.org/10.1023/A:1022556103536
Thomas DS, Eamus D (1999) The influence of predawn leaf water potential on stomatal responses to atmospheric water content at constant Ci and on stem hydraulic conductance and foliar ABA concentrations. J Exp Bot 50:243–251
Thomas DS, Eamus D (2002) Seasonal patterns of xylem sap pH, xylem abscisic acid concentration, leaf water potential and stomatal conductance of six evergreen and deciduous Australian savanna tree species. Aust J Bot 50:229–236
Thornthwaite CW, Mather JR (1955) The water balance. Publication in climatology. Drexel Institute of Technology, New Jersey, p 104
Tomlinson KW, Pooter L, Sterck FJ, Borghetti F, Ward D, Bie S, Langevelde F (2013) Leaf adaptations of evergreen and deciduous trees of semi-arid and humid savannas on three continents. J Ecol 101:430–440. https://doi.org/10.1111/1365-2745.12056
Wasternack C (2014) Action of jasmonates in plant stress responses and development-applied aspects. Biotechnol Adv 32:31–39. https://doi.org/10.1016/j.biotechadv.2013.09.009
Wilkinson S, Davies WJ (1997) Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol 113:559–573. https://doi.org/10.1104/pp.113.2.559