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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Croton blanchetianus modulates its morphophysiological responses to tolerate drought in a tropical dry forest

Keila R. Mendes A , João A. A. Granja A , Jean P. Ometto B , Antônio C. D. Antonino C , Rômulo S. C. Menezes C , Eugênia C. Pereira D E and Marcelo F. Pompelli A E
+ Author Affiliations
- Author Affiliations

A Plant Physiology Laboratory, Federal University of Pernambuco, Department of Botany, Recife, Pernambuco, Brazil.

B Brazilian Institute for Space Research, Remote Sensing Division, São José dos Campos, São Paulo, Brazil.

C Federal University of Pernambuco, Department of Nuclear Energy, Recife, Pernambuco, Brazil.

D Federal University of Pernambuco, Department of Geographical Sciences, Recife, Pernambuco, Brazil.

E Corresponding authors. Emails: marcelo.pompelli@ufpe.br; eugenia.pereira@pesquisador.cnpq.br

Functional Plant Biology 44(10) 1039-1051 https://doi.org/10.1071/FP17098
Submitted: 7 April 2017  Accepted: 28 June 2017   Published: 9 August 2017

Abstract

An understanding of variations in morphophysiological leaf traits of plant models in dry tropical forests is essential for quantifying C fluxes from forest ecosystems in response to climate changes. The present study evaluated the influences of seasonal rainfall and different light conditions on the gas exchange, nutrients, organic compounds and morphological traits in Croton blanchetianus Baill. trees within a fragment of Caatinga forest. Stomatal conductance (gs) and net photosynthesis (PN) demonstrated variations within the diurnal cycle, with maximum values at approximately midday and minimum values at predawn. The PN and the diurnal integrated CO2 assimilation were lower during the dry season than in the rainy season. Water use efficiency was positively correlated with PN (r = 0.73) during the dry season only. However, the correlation between PN and gs was observed during the rainy season only (r = 0.60). Thus we demonstrated that C. blanchetianus has a remarkable ability to adapt to global climatic changes and could be considered a model in studies exploring water relationships in woody plants; consequently, this species may be important in future reforestation studies.

Additional keywords: diurnal variation, gas exchange, leaf nutrient, morphological traits, seasonal variations.


References

Aasamaa K, Sõber A (2011) Stomatal sensitivities to changes in leaf water potential, air humidity, CO2 concentration and light intensity, and the effect of abscisic acid on the sensitivities in six temperate deciduous tree species. Environmental and Experimental Botany 71, 72–78.
Stomatal sensitivities to changes in leaf water potential, air humidity, CO2 concentration and light intensity, and the effect of abscisic acid on the sensitivities in six temperate deciduous tree species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WmtrjJ&md5=21b90c96fe4efd3938529bcd51bada2fCAS |

Amthor JS (2000) The McCree–de Wit–Penning de Vries–Thornley respiration paradigms: 30 years later. Annals of Botany 86, 1–20.
The McCree–de Wit–Penning de Vries–Thornley respiration paradigms: 30 years later.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlSntL8%3D&md5=9ac48ff73528840d7acdba25f7ae86acCAS |

Antunes WC, Mendes KR, Chaves ARM, Ometto JP, Jarma-Orozco A, Pompelli MF (2016) Spondias tuberosa trees grown in tropical, wet environments are more susceptible to drought than those grown in arid environments. Revista Colombiana de Ciencias Horticolas 10, 9–27.
Spondias tuberosa trees grown in tropical, wet environments are more susceptible to drought than those grown in arid environments.Crossref | GoogleScholarGoogle Scholar |

Arbona B, Manzi M, Ollas C, Gómez-Cadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. International Journal of Molecular Sciences 14, 4885–4911.
Metabolomics as a tool to investigate abiotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlt1Gjs7c%3D&md5=611a3865d31a159215d43eb26a0a2f95CAS |

Arve LE, Terfa MT, Gislerød HR, Olsen JE, Torre S (2013) High relative air humidity and continuous light reduce stomata functionality by affecting the ABA regulation in rose leaves. Plant, Cell & Environment 36, 382–392.
High relative air humidity and continuous light reduce stomata functionality by affecting the ABA regulation in rose leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjslWgtQ%3D%3D&md5=4012d1f925b6aa7d819461630ee0fd6cCAS |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlsVGitLk%3D&md5=7defff6fc79bf274d695d8ed5adb8abcCAS |

Bečková M, Gardian Z, Yu J, Konik P, Nixon PJ, Komenda J (2017) Association of Psb28 and Psb27 proteins with PSII–PSI supercomplexes upon exposure of Synechocystis sp. PCC 6803 to high light. Molecular Plant 10, 62–72.
Association of Psb28 and Psb27 proteins with PSII–PSI supercomplexes upon exposure of Synechocystis sp. PCC 6803 to high light.Crossref | GoogleScholarGoogle Scholar |

Bradford M (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
Rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2821bcfbf01a16b0f1b14eb3a73c5812CAS |

Brand MH (1997) Shade influences plant growth, leaf color and chlorophyll content of Kalmia latifolia L. cultivar. Horticultural Science 32, 206–208.

Buckley TN (2005) The control of stomata by water balance. New Phytologist 168, 275–292.
The control of stomata by water balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Smu7bI&md5=4139e1f3a622025141858b4c8dc15de3CAS |

Bullock SH, Mooney HA, Medina E (1995) ‘Seasonally dry tropical forests.’ (Cambridge University Press: Cambridge)

Campos MLO, Hsie BS, Granja JAA, Correia RM, Silva SRS, Almeida-Cortez JS, Pompelli MF (2012) Photosynthesis and antioxidant activity mechanisms in Jatropha curcas L. under salt stress. Brazilian Journal of Plant Physiology 24, 55–67.
Photosynthesis and antioxidant activity mechanisms in Jatropha curcas L. under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnt1Gisg%3D%3D&md5=03a85e175e8882eec904343d5cd88471CAS |

Chakraborty K, Mahatma M, Thawait L, Bishi S, Kalariya K, Singh A (2016) Water deficit stress affects photosynthesis and the sugar profile in source and sink tissues of groundnut (Arachis hypogaea L.) and impacts kernel quality. Journal of Applied Botany and Food Quality 89, 98–104.

Corcuera L, Morales F, Abadía A, Gil-Pelegrín E (2005) Seasonal changes in photosynthesis and photoprotection in a Quercus ilex subsp. ballota woodland located in its upper altitudinal extreme in the Iberian Peninsula. Tree Physiology 25, 599–608.
Seasonal changes in photosynthesis and photoprotection in a Quercus ilex subsp. ballota woodland located in its upper altitudinal extreme in the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlOlsro%3D&md5=69d7c61a6758467f774ad10ea1e4782aCAS |

DaMatta FM, Cunha RL, Antunes WC, Martins SCV, Araujo WL, Fernie AR, Moraes GABK (2008) In field-grown coffee trees source–sink manipulation alters photosynthetic rates, independently of carbon metabolism, via alterations in stomatal function. New Phytologist 178, 348–357.
In field-grown coffee trees source–sink manipulation alters photosynthetic rates, independently of carbon metabolism, via alterations in stomatal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls1Gqt7k%3D&md5=3b49698be15ec8a5d03dc1b74d47cfe0CAS |

Dantas JA, Bezerra Neto E, Barreto LP, Santos MVF (2006) Efeito da salinidade sobre o crescimento e composição mineral de seis clones de Pennisetum. Revista de Ciencias Agricolas 37, 97–101.

Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. The Plant Journal 4, 215–223.
Proline biosynthesis and osmoregulation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFyksbk%3D&md5=d508b038f8d5703bb863db349596cb87CAS |

Dias-Filho MB, Dawson TE (1995) Physiological responses to soil moisture stress in two Amazonian gap-invader species. Functional Ecology 9, 213–221.
Physiological responses to soil moisture stress in two Amazonian gap-invader species.Crossref | GoogleScholarGoogle Scholar |

DuBois M, Gilles KA, Hamilton JK, Reders PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
Colorimetric method for determination of sugars and related substances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG28XjvFynsg%3D%3D&md5=948f302e469f1432c943c1821b943cd8CAS |

Durand JL, Gonzalez-Dugo V, Gastal F (2010) How much do water deficits alter the nitrogen nutrition status of forage crops? Nutrient Cycling in Agroecosystems 88, 231–243.
How much do water deficits alter the nitrogen nutrition status of forage crops?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSjt7%2FN&md5=48932cf0e2a63cdc7d17b5ff8a97b5bbCAS |

Eamus D (1999) Ecophysiological traits of deciduous and evergreen woody species in the seasonally dry tropics. Trends in Ecology & Evolution 14, 11–16.
Ecophysiological traits of deciduous and evergreen woody species in the seasonally dry tropics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbgsVejuw%3D%3D&md5=87a95039e6f67299d5fb82b7e88c9d11CAS |

Ehleringer JR (1991) 13C/12C fractionation and its utility in terrestreial plant studies. In ‘Carbon isotope techniques’. (Eds DC Coleman, B Fry) pp. 187–200. (Academic Press: New York)

Ehleringer JR, Cooper TA (1988) Correlations between carbon isotope ratio and microhabitat in desert plants. Oecologia 76, 562–566.
Correlations between carbon isotope ratio and microhabitat in desert plants.Crossref | GoogleScholarGoogle Scholar |

Ehleringer JR, Phillips SL, Comstock JP (1992) Seasonal variation in the carbon isotopic composition of desert plants. Functional Ecology 6, 396–404.
Seasonal variation in the carbon isotopic composition of desert plants.Crossref | GoogleScholarGoogle Scholar |

Faraloni C, Cutino I, Petruccelli R, Leva AR, Lazzeri S, Torzillo G (2011) Chlorophyll fluorescence technique as a rapid tool for in vitro screening of olive cultivars (Olea europaea L.) tolerant to drought stress. Environmental and Experimental Botany 73, 49–56.
Chlorophyll fluorescence technique as a rapid tool for in vitro screening of olive cultivars (Olea europaea L.) tolerant to drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGgtLfJ&md5=3ddfe18895be4d413ff32b0967fe7a83CAS |

Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
On the relationship between carbon isotope discrimination and intercellular carbon dioxide concentration in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhsF2ms70%3D&md5=03f744f647b86a456f10798ed5446470CAS |

Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Annals of Botany 89, 183–189.
Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslymsLs%3D&md5=89d0952cc5dabe59e7d64a5e7ecac009CAS |

Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbo M (2006) Kepping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiologia Plantarum 127, 343–352.
Kepping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhu7o%3D&md5=f33d3d5a29c9759f29ee6c21e6c322f7CAS |

Flexas J, Díaz-Espejo A, Conesa MA, Coopman RE, Douthe C, Gago J, Gallé A, Galmés J, Medrano H, Ribas-Carbo M, Tomàs M, Niinemets Ü (2016) Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. Plant, Cell & Environment 39, 965–982.
Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlvVaitLo%3D&md5=f7c00b80d5c28686c57d9a5ac4e2074fCAS |

Foley JA, Levis S, Costa MH, Cramer W, Pollard D (2000) Incorporating dynamic vegetation cover within global climate models. Ecological Applications 10, 1620–1632.
Incorporating dynamic vegetation cover within global climate models.Crossref | GoogleScholarGoogle Scholar |

Fyllas NM, Patiño S, Baker TR, Nardoto GB, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jiménez EM, Luizão DA, Neill DA, Silva N, Prieto A, Rudas A, Silveira M, Vieira ICG, Lopez-Gonzales G, Malhi Y, Phillips OL, Lloyd J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6, 2677–2708.
Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate.Crossref | GoogleScholarGoogle Scholar |

Giday H, Kjaer KH, Fanourakis D, Ottosen C-O (2013) Smaller stomata require less severe leaf drying to close: a case study in Rosa hydrida. Journal of Plant Physiology 170, 1309–1316.
Smaller stomata require less severe leaf drying to close: a case study in Rosa hydrida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVGjtL4%3D&md5=d8b2f7207ea5e82b41d78c0972dd2a77CAS |

Gitelson AA, Gamon JA, Solovchenko A (2017) Multiple drivers of seasonal change in PRI: implications for photosynthesis 1. Leaf level. Remote Sensing of Environment 191, 110–116.
Multiple drivers of seasonal change in PRI: implications for photosynthesis 1. Leaf level.Crossref | GoogleScholarGoogle Scholar |

Gonzalez-Dugo V, Durand JL, Gastal F, Bariac T, Poincheval J (2012) Restricted root-to-shoot translocation and decreased sink size are responsible for limited nitrogen uptake in three grass species under water deficit. Environmental and Experimental Botany 75, 258–267.
Restricted root-to-shoot translocation and decreased sink size are responsible for limited nitrogen uptake in three grass species under water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFSksb3P&md5=890a375a4fb54ebd75c8889bdae54b90CAS |

Gupta N, Thind SKT, Bains NS (2014) Glycine betaine application modifies biochemical attributes of osmotic adjustment in drought stressed wheat. Plant Growth Regulation 72, 221–228.
Glycine betaine application modifies biochemical attributes of osmotic adjustment in drought stressed wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1SrsbbK&md5=bcd5546c8bfd754c375eab48d0992e87CAS |

Güsewell SN (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266.
N : P ratios in terrestrial plants: variation and functional significance.Crossref | GoogleScholarGoogle Scholar |

Hardoon DR, Szedmak S, Shawe-Taylor J (2004) Canonical correlation analysis: an overview with application to learning methods. Neural Computation 16, 2639–2664.
Canonical correlation analysis: an overview with application to learning methods.Crossref | GoogleScholarGoogle Scholar |

Hikosaka K (2004) Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. Journal of Plant Research 117, 481–494.
Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance.Crossref | GoogleScholarGoogle Scholar |

HongBo S, ZongSuo L, MingAn S (2006) Osmotic regulation of 10 wheat (Triticum aestivum L.) genotypes at soil water deficits. Colloids and Surfaces. B, Biointerfaces 47, 132–139.
Osmotic regulation of 10 wheat (Triticum aestivum L.) genotypes at soil water deficits.Crossref | GoogleScholarGoogle Scholar |

Hsie BS, Mendes KR, Antunes WC, Endres L, Campos MLO, Souza FC, Santos ND, Singh B, Arruda ECP, Pompelli MF (2015) Jatropha curcas L. (Euphorbiaceae) modulates stomatal traits in response to leaf-to-air vapor pressure deficit. Biomass and Bioenergy 81, 273–281.
Jatropha curcas L. (Euphorbiaceae) modulates stomatal traits in response to leaf-to-air vapor pressure deficit.Crossref | GoogleScholarGoogle Scholar |

Ishida A, Toma T (1999) Limitation of leaf carbon gain by stomatal and photochemical processes in the top canopy of Macaranga conifera, a tropical pioneer tree. Tree Physiology 19, 467–473.
Limitation of leaf carbon gain by stomatal and photochemical processes in the top canopy of Macaranga conifera, a tropical pioneer tree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVeitbg%3D&md5=14627950fb67d3969e904e90f29de940CAS |

Keenan T, Sabate S, Gracia C (2010) The importance of mesophyll conductance in regulating forest ecosystem productivity during drought periods. Global Change Biology 16, 1019–1034.
The importance of mesophyll conductance in regulating forest ecosystem productivity during drought periods.Crossref | GoogleScholarGoogle Scholar |

Köppen W (1948) ‘Climatologia: con un estudio de los climas de la tierra.’ (Fondo de Cultura Economica: Mexico)

Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. Journal of Experimental Botany 56, 337–346.
Singlet oxygen production in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovVymsg%3D%3D&md5=0f7a8874b5132e8e640bee5a025ff9d0CAS |

Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Annals of Botany 103, 561–579.
Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7g%3D&md5=73e2e251fc4600011f08a0ead31d5405CAS |

Lichtenthaler HK, Ac A, Marek MV, Kalina J, Urban O (2007) Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiology and Biochemistry 45, 577–588.
Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot12qsLs%3D&md5=3ed9f0f8577f9d12bc99325b487a7330CAS |

Lloyd J, Farqhar GD (2008) Effects of rising temperatures and [CO2] on the physiology of tropical forest tree. Philosophical Transactions of the Royal Society B 363, 1811–1817.
Effects of rising temperatures and [CO2] on the physiology of tropical forest tree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFGqt7w%3D&md5=6ddb0ea5ec2458459868b9d7d2462febCAS |

Marengo JA, Ambrizzi T, Rocha RP, Alves LM, Cuadra SV, Valverde MC, Torres RR, Santos DC, Ferraz SET (2010) Future change of climate in South America in the late twenty-first century: intercomparison of scenarios from three regional climate models. Climate Dynamics 35, 1073–1097.
Future change of climate in South America in the late twenty-first century: intercomparison of scenarios from three regional climate models.Crossref | GoogleScholarGoogle Scholar |

Marengo JA, Chou SC, Kay G, Alves LM, Pesquero JF, Soares WR, Santos DC, Lyra AA, Sueiro G, Betts R, Chagas DJ, Gomes JL, Bustamante JF, Tavares P (2012) Development of regional future climate change scenarios in South America using the Eta CPTEC/HadCM3 climate change projections: climatology and regional analyses for the Amazon, São Francisco and the Paraná River basins. Climate Dynamics 38, 1829–1848.
Development of regional future climate change scenarios in South America using the Eta CPTEC/HadCM3 climate change projections: climatology and regional analyses for the Amazon, São Francisco and the Paraná River basins.Crossref | GoogleScholarGoogle Scholar |

Markesteijn L, Poorter L, Bongers F (2007) Light-dependent leaf trait variation in 43 tropical dry forest tree species. American Journal of Botany 94, 515–525.
Light-dependent leaf trait variation in 43 tropical dry forest tree species.Crossref | GoogleScholarGoogle Scholar |

Martin B, Ruiz-Torres NA (1992) Effects of water-deficit stress on photosynthesis, its components and component limitations, and on water use efficiency in wheat (Triticum aestivum L.). Plant Physiology 100, 733–739.
Effects of water-deficit stress on photosynthesis, its components and component limitations, and on water use efficiency in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmsVykt70%3D&md5=7c3063c909c99a7d175b2dfea7e91511CAS |

Martínez DE, Guiamet JJG (2004) Distortion of the SPAD 502 chlorophyll meter readings by changes in irradiance and leaf water status. Agronomie 24, 41–46.
Distortion of the SPAD 502 chlorophyll meter readings by changes in irradiance and leaf water status.Crossref | GoogleScholarGoogle Scholar |

Mendes KR, Marenco RA (2014) Is stomatal conductance of Central Amazonian saplings influenced by circadian rhythms under natural conditions? Theoretical and Experimental Plant Physiology 26, 115–125.
Is stomatal conductance of Central Amazonian saplings influenced by circadian rhythms under natural conditions?Crossref | GoogleScholarGoogle Scholar |

Mendes KR, Marenco RA (2015) Photosynthetic traits of tree species in response to leaf nutrient content in the central Amazon. Theoretical and Experimental Plant Physiology 27, 51–59.
Photosynthetic traits of tree species in response to leaf nutrient content in the central Amazon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1Wku7jE&md5=1a58b8a3be4ef884accaed2f3b712b24CAS |

Mlinarić S, Dunić JA, Babojelić MS, Cesar V, Lepeduš H (2017) Differential accumulation of photosynthetic proteins regulates diurnal photochemical adjustments of PSII in common fig (Ficus carica L.) leaves. Journal of Plant Physiology 209, 1–10.
Differential accumulation of photosynthetic proteins regulates diurnal photochemical adjustments of PSII in common fig (Ficus carica L.) leaves.Crossref | GoogleScholarGoogle Scholar |

Moore S, Stein WH (1954) A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. The Journal of Biological Chemistry 221, 907–913.

Mott KA, Peak D (2010) Stomatal responses to humidity and temperature in darkness. Plant, Cell & Environment 33, 1084–1090.

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta 1767, 414–421.
Photoinhibition of photosystem II under environmental stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1ygsLw%3D&md5=92714112509f50441fc04f006ffa4bcdCAS |

Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: Re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochimica et Biophysica Acta 1817, 1127–1133.
The mechanism of photoinhibition in vivo: Re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xkt1Ghsbg%3D&md5=f4249851e6c8dcdf410b16e55864d3f5CAS |

Murray-Tortarolo G, Friedlingstein P, Sitch S, Seneviratne S, Fletcher I, Mueller B, Greve P, Anav A, Liu Y, Ahlström A, Huntingford C, Levis S, Levy P, Lomas M, Poulter B, Viovy N, Zaehle S, Zeng N (2016) Changes in the dry season intensity are a key driver of regional NPP trends. Geophysical Research Letters 43, 2632–2639.
Changes in the dry season intensity are a key driver of regional NPP trends.Crossref | GoogleScholarGoogle Scholar |

Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta 1757, 742–749.
A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotVCrsb4%3D&md5=0cf0ac489a9d1bf87b4a834e22161d84CAS |

Nouvellon Y, Laclau JP, Epron D, Kinana A, Mabiala A, Roupsard O, Bonnefond JM, Le Maire G, Marsden C, Bontemps JD, Saint-André L (2010) Within-stand and seasonal variations of specific leaf area in a clonal Eucalyptus plantation in the Republic of Congo. Forest Ecology and Management 259, 1796–1807.
Within-stand and seasonal variations of specific leaf area in a clonal Eucalyptus plantation in the Republic of Congo.Crossref | GoogleScholarGoogle Scholar |

Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell & Environment 28, 916–927.
Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees.Crossref | GoogleScholarGoogle Scholar |

Parker G, Tinoco-Ojanguren C, Martinez-Yrizar A, Maass M (2005) Seasonal balance and vertical pattern of photosynthetically active radiation within canopies of a tropical dry deciduous forest ecosystem in Mexico. Journal of Tropical Ecology 21, 283–295.
Seasonal balance and vertical pattern of photosynthetically active radiation within canopies of a tropical dry deciduous forest ecosystem in Mexico.Crossref | GoogleScholarGoogle Scholar |

Peak D, Mott KA (2011) A new, vapour-phase mechanism for stomatal responses to humidity and temperature. Plant, Cell & Environment 34, 162–178.
A new, vapour-phase mechanism for stomatal responses to humidity and temperature.Crossref | GoogleScholarGoogle Scholar |

Pereira MPS, Justino F, Malhado ACM, Barbosa H, Marengo JA (2014) The influence of oceanic basins on drought and ecosystem dynamics in northeast Brazil. Environmental Research Letters 9, 124013
The influence of oceanic basins on drought and ecosystem dynamics in northeast Brazil.Crossref | GoogleScholarGoogle Scholar |

Pompelli MF, Barata-Luís RM, Vitorino HS, Gonçalves ER, Rolim EV, Santos MG, Almeida-Cortez JS, Endres L (2010a) Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery. Biomass and Bioenergy 34, 1207–1215.
Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVWmur8%3D&md5=8355484d932017ba34d171ff2ade8078CAS |

Pompelli MF, Ferreira DTRG, Cavalcante PPGS, Salvador TL, Hsie BS, Endres L (2010b) Environmental influence on the physico-chemical and physiological properties of Jatropha curcas L. seeds. Australian Journal of Botany 58, 421–427.
Environmental influence on the physico-chemical and physiological properties of Jatropha curcas L. seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFaiu7nM&md5=7aed6798eb40d468025c99263c6d59daCAS |

Pompelli MF, Martins SCV, Antunes WC, Chaves ARM, DaMatta FM (2010c) Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. Journal of Plant Physiology 167, 1052–1060.
Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsVCltLY%3D&md5=00d4577762c76c494adbe23d40527307CAS |

Pompelli MF, França SCS, Tigre RC, Oliveira MT, Sacilot M, Pereira ECG (2013) Spectrophotometric determinations of chloroplastidic pigments in acetone, ethanol and dimethylsulphoxide. Brazilian Journal of Biological Sciences 11, 52–58.

Ribeiro RV, Machado EC, Santos MG, Oliveira RF (2009) Photosynthesis and water relations of well-watered orange plants as affected by winter and summer conditions. Photosynthetica 47, 215–222.
Photosynthesis and water relations of well-watered orange plants as affected by winter and summer conditions.Crossref | GoogleScholarGoogle Scholar |

Rosas-Anderson P, Shekoofa A, Sinclair TR, Balota M, Isleib TG, Tallury S, Rufty T (2014) Genetic variation in peanut leaf maintenance and transpiration recovery from severe soil drying. Field Crops Research 158, 65–72.
Genetic variation in peanut leaf maintenance and transpiration recovery from severe soil drying.Crossref | GoogleScholarGoogle Scholar |

Santos ACJ, Melo JIM (2010) Flora vascular de uma área de caatinga no estado da Paraíba – Nordeste do Brasil. Revista Caatinga 23, 32–40.

Santos MG, Oliveira MT, Figueiredo KV, Falcão HM, Arruda ECP, Almeida-Cortez JS, Sampaio EVSB, Ometto JPHB, Menezes RSC, Oliveira AFM, Pompelli MF, Antonino ACD (2014) Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes? Theoretical and Experimental Plant Physiology 26, 83–99.
Caatinga, the Brazilian dry tropical forest: can it tolerate climate changes?Crossref | GoogleScholarGoogle Scholar |

Scoffoni C, Kunkle J, Pasquet-Kok J, Vuong C, Patel AM, Montgomery RA, Givnish TJ, Sack L (2015) Light-induced plasticity in leaf hydraulics, venation, anatomy, and gas exchange in ecologically diverse Hawaiian lobeliads. New Phytologist 207, 43–58.
Light-induced plasticity in leaf hydraulics, venation, anatomy, and gas exchange in ecologically diverse Hawaiian lobeliads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpsVSqu7g%3D&md5=3fe84b8167368225a8394b7c2c4b4225CAS |

Shangguan Z, Shao M, Dyckmans J (2000) Nitrogen nutrition and water stress effects on leaf photosynthetic gas exchange and water use efficiency in winter wheat. Environmental and Experimental Botany 44, 141–149.
Nitrogen nutrition and water stress effects on leaf photosynthetic gas exchange and water use efficiency in winter wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtlGmtrY%3D&md5=2886c7db86178e1df5a85a12ec917727CAS |

Shao HB, Chu L-Y, Jaleel CA, Zhao D (2008) Water-deficit stress-induced anatomical changes in higher plants. Comptes Rendus Biologies 331, 215–225.
Water-deficit stress-induced anatomical changes in higher plants.Crossref | GoogleScholarGoogle Scholar |

Signarbieux C, Feller U (2011) Nonstomatal limitations of photosynthesis in grassland species under artificial drought in the field. Environmental and Experimental Botany 71, 192–197.
Nonstomatal limitations of photosynthesis in grassland species under artificial drought in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFWitrc%3D&md5=235901555c6d173859943fd197e59696CAS |

Silva FC (2009) ‘Manual de análises químicas de solos, plantas e fertilizantes, 2. ed.’ (Embrapa Informação Tecnológica: Brasília)

Silva EN, Silva SLF, Viégas RA, Silveira JAG (2010) The role of organic and inorganic solutes in the osmotic adjustment of drought-stressed Jatropha curcas plants. Environmental and Experimental Botany 69, 279–285.
The role of organic and inorganic solutes in the osmotic adjustment of drought-stressed Jatropha curcas plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWls74%3D&md5=05ead40fc86e0e5d2a5056b7558e7b21CAS |

   (a) Singh AL (2004) Groundnut research in India. In ‘Growth and physiology of groundnut. Vol. 6’. (Eds MS Basu, NB Singh) pp. 178–212. (National Research Centre for Groundnut (ICAR): Jodhpur)
      Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401, 914–917.
Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP.Crossref | GoogleScholarGoogle Scholar |

Warren CR, Adams MA (2004) Evergreen trees do not maximize instantaneous photosynthesis. Trends in Plant Science 9, 270–274.
Evergreen trees do not maximize instantaneous photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVemtbk%3D&md5=6db136fb45cc97505eb01d5468214ff0CAS |

Winter K (1981) CO2 and water vapour exchange, malate content and δ13C value in Cicer arietinum grown under two water regimes. Zeitschrift für Pflanzenphysiologie 101, 421–430.
CO2 and water vapour exchange, malate content and δ13C value in Cicer arietinum grown under two water regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXkslKqtLs%3D&md5=13030dc096f0bbab2360558461d3f24bCAS |

Winter K, Osmond CB, Pate JS (1981) Coping with salinity. In ‘Biology of Australian native plants’. (Eds JS Pate, AJ McComb) pp. 88–113. (University of Western Australia Press: Perth, Australia)

Zhou S, Duursma RA, Medlyn BE, Kelly JWG, Prentice IC (2013) How should we model plant responses to drought? An analysis of stomatal and non-stomatal responses to water stress. Agricultural and Forest Meteorology 20, 84–94.