Resilience of a semi-deciduous shrub, Cistus salvifolius, to severe summer drought and heat stress
Olga M. Grant A B F , Łukasz Tronina A , José I. García-Plazaola D , Raquel Esteban C D , João Santos Pereira E and M. Manuela Chaves A EA Laboratório de Ecofisiologia Molecular, Instituto de Tecnologia Química e Biológica, Quinta do Marquês, 2784-505 Oeiras, Portugal.
B UCD Forestry, University College Dublin, Belfield, Dublin 4, Ireland.
C ZTF-FTC, Universidad del País Vasco (UPV/EHU), Barrio Sarriena s/n, 48940 Leioa – Bizkaia, Spain.
D Agrobiotechnology Institute. IdAB-CSIC-UPNA, E- 31192 Mutilva, Navarra, Spain.
E Instituto Superior de Agronomia, Universidade Técnica de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal.
F Corresponding author. Email: olga.grant@ucd.ie
Functional Plant Biology 42(2) 219-228 https://doi.org/10.1071/FP14081
Submitted: 12 March 2014 Accepted: 26 August 2014 Published: 24 September 2014
Abstract
Shrubs often form the understorey in Mediterranean oak woodlands. These shrubs are exposed to recurrent water deficits, but how they will respond to predicted future exacerbation of drought is not yet understood. The ecophysiology of the shrub Cistus salvifolius L. was studied over the summer of 2005, which was during a heat-wave superimposed on the most severe drought in the Iberian Peninsula in the last 140 years. Branch water potential fell drastically during the summer, accompanied by stomatal closure and downregulation of PSII, with a concomitant loss of chlorophyll in the leaves. A parallel increase in the ratio of light-dissipating to light-capturing pigments and the proportion of xanthophyll cycle pigments in the de-epoxidated state, along with alterations in the structure of the light harvesting complex, may have reduced the potential for damage to leaves. Substantial increases in leaf tocopherol content during high radiation may have reduced damage from free radicals. Following autumn rains, leaves of the same shrubs showed physiological recovery, indicating the resilience of this Mediterranean species, for which an extremely dry hydrological year with 45% less rainfall than average, did not prevent healthy leaf functioning in response to renewed soil moisture availability.
Additional keywords: antioxidants, chlorophyll fluorescence, photosystem II, thermography, water potential, xanthophyll cycle.
References
Abbasi A-R, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2007) Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiology 143, 1720–1738.| Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFWjtLc%3D&md5=0c19761ef158fd953e4a2037a0690f39CAS | 17293434PubMed |
Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489–504.
| Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins.Crossref | GoogleScholarGoogle Scholar | 24233012PubMed |
Björkman O, Powles SB (1984) Inhibition of photosynthetic reactions under water stress: interactions with light level. Planta 161, 490–504.
| Inhibition of photosynthetic reactions under water stress: interactions with light level.Crossref | GoogleScholarGoogle Scholar | 24253918PubMed |
Bugalho M, Plieninger T, Aronson J, Ellatifi M, Crespo D (2009) Open woodlands: a diversity of uses (and overuses). In ‘Cork oak woodlands on the edge: conservation, adaptive management and restoration’. (Eds J Aronson, JS Pereira, JG Pausas) pp. 34–45. (Island Press: Washington, DC)
Correia OA, Catarino FM (1994) Seasonal changes in soil-to-leaf resistance in Cistus sp. and Pistacia lentiscus. Acta Oecologica 15, 289–300.
Correia OA, Catarino FM, Tenhunen JD, Lange OL (1987) Regulation of water use by four species of Cistus in the scrub vegetation of the Serra da Arrábida, Portugal. In ‘Plant response to stress. Functional analysis in Mediterranean ecosystems’. (Eds JD Tenhunen, FM Catarino, OL Lange, WC Oechel) pp. 247–258. (Springer-Verlag: Berlin)
Correia OA, Martins AC, Catarino FM (1992) Comparative phenology and seasonal foliar nitrogen variation in Mediterranean species of Portugal. Ecologia Mediterranea 18, 7–18.
Correia AC, Costa e Silva F, Correia AV, Hussain MZ, Rodrigues AD, David JS, Pereira JS (2014) Carbon sink strength of a Mediterranean cork oak understorey: how do semi-deciduous and evergreen shrubs face summer drought? Journal of Vegetation Science 25, 411–426.
| Carbon sink strength of a Mediterranean cork oak understorey: how do semi-deciduous and evergreen shrubs face summer drought?Crossref | GoogleScholarGoogle Scholar |
Costa JM, Grant OM, Chaves MM (2013) Thermography to explore plant-environment interactions. Journal of Experimental Botany 64, 3937–3949.
| Thermography to explore plant-environment interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1SmtLbK&md5=10a95866aac673bb305b1e450e1381b4CAS | 23599272PubMed |
David TS, Pinto CA, Nadezhdina N, Kurz-Besson C, Henriques MO, Quilhó T, Cermak J, Chaves MM, Pereira JS, David JS (2013) Root functioning, tree water use and hydraulic redistribution in Quercus suber trees: a modeling approach based on root sap flow. Forest Ecology and Management 307, 136–146.
| Root functioning, tree water use and hydraulic redistribution in Quercus suber trees: a modeling approach based on root sap flow.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use-efficiency of wheat genotypes. Australian Journal of Plant Physiology 11, 539–552.
| Isotopic composition of plant carbon correlates with water-use-efficiency of wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFSju7w%3D&md5=3cd5cbba90ce8383b6cdde062d61e7f7CAS |
Galle A, Florez-Sarasa I, El Aououad H, Flexas J (2011) The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles. Journal of Experimental Botany 62, 5207–5216.
| The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejsrbJ&md5=837baba7ea72c93191ecf55986efb30eCAS | 21813795PubMed |
García-Herrera R, Paredes D, Trigo RM, Trigo IF, Hernandez E, Barriopedro D, Mendes MA (2007) The outstanding 2004/05 drought in the Iberian Peninsula: associated atmospheric circulation. Journal of Hydrometeorology 8, 483–498.
| The outstanding 2004/05 drought in the Iberian Peninsula: associated atmospheric circulation.Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI, Becerril JM (2001) Seasonal changes in photosynthetic pigments and antioxidants in beech (Fagus sylvatica) in a Mediterranean climate: implications for tree decline diagnosis. Australian Journal of Plant Physiology 28, 225–232.
García-Plazaola JI, Esteban R, Hormaetxe K, Fernández-Marin B, Becerril JM (2008) Photoprotective responses of Mediterranean and Atlantic trees to the extreme heat-wave of summer 2003 in Southwestern Europe. Trees 22, 385–392.
| Photoprotective responses of Mediterranean and Atlantic trees to the extreme heat-wave of summer 2003 in Southwestern Europe.Crossref | GoogleScholarGoogle Scholar |
Grant OM, Incoll LD (2005) Photochemical efficiency is an important component of ecophysiological variation of Cistus albidus between habitats in south-east Spain. Functional Plant Biology 32, 107–115.
| Photochemical efficiency is an important component of ecophysiological variation of Cistus albidus between habitats in south-east Spain.Crossref | GoogleScholarGoogle Scholar |
Grant OM, Incoll LD, McNeilly T (2005) Variation in growth responses to availability of water in Cistus albidus populations from different habitats. Functional Plant Biology 32, 817–829.
| Variation in growth responses to availability of water in Cistus albidus populations from different habitats.Crossref | GoogleScholarGoogle Scholar |
Grant OM, Tronina Ł, Ramalho JC, Besson CK, Lobo-Do-Vale R, Pereira JS, Jones HG, Chaves MM (2010) The impact of drought on leaf physiology of Quercus suber L. trees: comparison of an extreme drought event with chronic rainfall reduction. Journal of Experimental Botany 61, 4361–4371.
| The impact of drought on leaf physiology of Quercus suber L. trees: comparison of an extreme drought event with chronic rainfall reduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlShtLbE&md5=bede0c296b643467b8de2c592fc846cbCAS | 20685731PubMed |
Gulías J, Cife J, Jonasson S, Medrano H, Flexas J (2009) Seasonal and inter-annual variations of gas exchange in thirteen woody species along a climatic gradient in the Mediterranean island of Mallorca. Flora 204, 169–181.
| Seasonal and inter-annual variations of gas exchange in thirteen woody species along a climatic gradient in the Mediterranean island of Mallorca.Crossref | GoogleScholarGoogle Scholar |
IPCC-WGI
Jones HG (1999) Use of infrared thermometry for estimation of stomatal conductance as a possible aid to irrigation scheduling. Agricultural and Forest Meteorology 95, 139–149.
| Use of infrared thermometry for estimation of stomatal conductance as a possible aid to irrigation scheduling.Crossref | GoogleScholarGoogle Scholar |
Jones HG, Stoll M, Santos T, de Sousa C, Chaves MM, Grant OM (2002) Use of infrared thermography for monitoring stomatal closure in the field: application to grapevine. Journal of Experimental Botany 53, 1–12.
Karavatas S, Manetas Y (1999) Seasonal pattern of photosystem 2 photochemical efficiency in evergreen sclerophylls and drought semi-deciduous shrubs under Mediterranean field conditions. Photosynthetica 36, 41–49.
| Seasonal pattern of photosystem 2 photochemical efficiency in evergreen sclerophylls and drought semi-deciduous shrubs under Mediterranean field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltlOnsb4%3D&md5=75c48bdfd0acb8f1d566fdf4e74b13b4CAS |
Kurz Besson C, Lobo-do-Vale R, Rodrigues ML, Almeida P, Herd A, Grant OM, David TS, Schmidt M, Otieno D, Keenan TF, Gouveia C, Mériaux C, Chaves MM, Pereira JS (2014) Cork oak physiological responses to manipulated water availability in a Mediterranean woodland. Agricultural and Forest Meteorology 184, 230–242.
| Cork oak physiological responses to manipulated water availability in a Mediterranean woodland.Crossref | GoogleScholarGoogle Scholar |
Matsubara S, Morosinotto T, Osmond CB, Bassi R (2007) Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes. Plant Physiology 144, 926–941.
| Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvValt7k%3D&md5=bbf30719d8a8b3ef60795865b734188aCAS | 17384157PubMed |
Miranda PMA, Valente MA, Tomé AR, Trigo R, Coelho MFES, Aguiar A, Azevedo EB (2006) O clima de Portugal nos séculos XX e XXI. In ‘Alterações Climáticas em Portugal. Cenários, Impactes e Medidas de Adaptação.’ (Eds FD Santos, P Miranda) pp. 45–113. (Gradiva: Lisboa, Portugal)
Munné-Bosch S, Alegre L (2000) The significance of β-carotene, α-tocopherol and the xanthophyll cycle in droughted Melissa officinalis plants. Australian Journal of Plant Physiology 27, 139–146.
Munné-Bosch S, Schwarz K, Alegre L (1999) Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants. Plant Physiology 121, 1047–1052.
| Enhanced formation of α-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants.Crossref | GoogleScholarGoogle Scholar | 10557254PubMed |
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. Journal of Experimental Botany 64, 3983–3998.
| Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1SmtLbJ&md5=16bc48a3feb442c8496d82e0ee055552CAS | 23913954PubMed |
Niyogi KK, Björkman O, Grossmann AR (1997) The roles of specific xanthophylls in photoprotection. Proceedings of the National Academy of Sciences of the United States of America 94, 14162–14167.
| The roles of specific xanthophylls in photoprotection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s7nvVKnuw%3D%3D&md5=974c342f67ad9c04395bdc01786ef469CAS | 9391170PubMed |
Núñez-Olivera E, Martínez-Abaigar J, Escudero JC (1996) Adaptability of leaves of Cistus ladanifer to widely varying environmental conditions. Functional Ecology 10, 636–646.
| Adaptability of leaves of Cistus ladanifer to widely varying environmental conditions.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Lloret F, Montoya R (2001) Severe drought effects on Mediterranean woody flora in Spain. Forest Science 47, 214–218.
Ramalho JC, Zlatev ZS, Leitão AE, Pais IP, Fortunato AS, Lidon FC (2014) Moderate water stress causes different stomatal and non-stomatal changes in the photosynthetic functioning of Phaseolus vulgaris L. genotypes. Plant Biology 16, 133–146.
| Moderate water stress causes different stomatal and non-stomatal changes in the photosynthetic functioning of Phaseolus vulgaris L. genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXksFSi&md5=283134698aabe0764714d9c943239902CAS |
Trebst A (2003) Function of β-carotene and tocopherol in photosystem II. Zeitschrift für Naturforschung 58c, 609–620.
Werner C, Correia O, Beyschlag W (2002) Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. Functional Plant Biology 29, 999–1011.
| Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem.Crossref | GoogleScholarGoogle Scholar |
Zunzunegui M, Díaz Barradas MC, Ain-Lhout F, Clavijo A, García Novo F (2005) To live or to survive in Doñana dunes: adaptive responses of woody species under a Mediterranean climate. Plant and Soil 273, 77–89.
| To live or to survive in Doñana dunes: adaptive responses of woody species under a Mediterranean climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1Ojs7g%3D&md5=d941e470d5143b3fe5cb32ed0d2c9853CAS |
Zunzunegui M, Díaz Barradas MC, Ain-Lhout F, Alvarez-Cansino L, Esquivias MP, García Novo F (2011) Seasonal physiological plasticity and recovery capacity after summer stress in Mediterranean scrub communities. Plant Ecology 212, 127–142.
| Seasonal physiological plasticity and recovery capacity after summer stress in Mediterranean scrub communities.Crossref | GoogleScholarGoogle Scholar |