Photosynthetic performance and biochemical adjustments in two co-occurring Mediterranean evergreens, Quercus ilex and Arbutus unedo, differing in salt-exclusion ability
Lina Fusaro A , Simone Mereu B , Cecilia Brunetti C , Martina Di Ferdinando C , Francesco Ferrini C , Fausto Manes A , Elisabetta Salvatori A , Riccardo Marzuoli D , Giacomo Gerosa D and Massimiliano Tattini E F
+ Author Affiliations
- Author Affiliations
A Department of Environmental Biology, Sapienza University of Rome, P.le Aldo Moro, 5 - 00185, Rome, Italy.
B Department of Science for Nature and Environmental Resources (DipNET), University of Sassari, Piazza Università 21 - 07100, Sassari, Italy.
C Department of Agri-Food Production and Environmental Sciences, University of Florence, Viale delle Idee 30, 50019, Sesto Fiorentino, Florence, Italy.
D Department of Mathematic and Physic, Catholic University of Brescia, Via Musei 41 - 25121 Brescia, Italy.
E The National Research Council of Italy, Department of Biology, Agriculture and Food Sciences, Institute for Plant Protection, Via Madonna del Piano 10, I-50 019, Sesto Fiorentino, Florence, Italy.
F Corresponding author. Email: tattini@ipp.cnr.it
Functional Plant Biology 41(4) 391-400 https://doi.org/10.1071/FP13241
Submitted: 8 August 2013 Accepted: 20 October 2013 Published: 28 November 2013
Abstract
The responses to mild root zone salinity stress were investigated in two co-occurring Mediterranean woody evergreens, Quercus ilex L. and Arbutus unedo L., which differ in morpho-anatomical traits and strategies to cope with water deficit. The aim was to explore their strategies to allocate potentially toxic ions at organism level, and the consequential physiological and biochemical adjustments. Water and ionic relations, gas exchange and PSII performance, the concentration of photosynthetic pigments, and the activity of antioxidant defences, were measured. Q. ilex displayed a greater capacity to exclude Na+ and Cl– from the leaf than A. unedo, in part as a consequence of greater reductions in transpiration rates. Salt-induced reductions in CO2 assimilation resulted in Q. ilex suffering from excess of light to a greater extent than A. unedo. Consistently, in Q. ilex effective mechanisms of nonphotochemical quenching, also sustained by the lutein epoxide-lutein cycle, operated in response to salinity stress. Q. ilex also displayed a superior capacity to detoxify reactive oxygen species (ROS) than A. unedo. Our data suggest that the ability to exclude salt from actively growing shoot organs depends on the metabolic cost of sustaining leaf construction, i.e. species-specific leaf life-span, and the relative strategies to cope with salt-induced water stress. We discuss how contrasting abilities to restrict the entry and transport of salt in sensitive organs relates with species-specific salt tolerance.
Additional keywords: leaf longevity, net ion fluxes, salt tolerance, stomatal conductance, violaxanthin-cycle pigments, water relations.
References
Alessio GA, de Lillis M, Brugnoli E, Lauteri M (2004) Water sources and water-use efficiency in Mediterranean coastal dune vegetation. Plant Biology 6, 350–357.| Water sources and water-use efficiency in Mediterranean coastal dune vegetation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c3ksVOktQ%3D%3D&md5=e0251118c6ca62eebce6f27882ec6ebfCAS | 15143444PubMed |
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
| Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=bb62c10883f0f45b9778cbbe05a12a70CAS | 15377225PubMed |
Beckett M, Loreto F, Velikova V, Brunetti C, Di Ferdinando M, Tattini M, Calfapietra C, Farrant JM (2012) Photosynthetic limitations and volatile and non-volatile isoprenoids in the poikilochlorophyllous resurrection plant Xerophyta humilis during dehydration and rehydration. Plant, Cell & Environment 35, 2061–2074.
| Photosynthetic limitations and volatile and non-volatile isoprenoids in the poikilochlorophyllous resurrection plant Xerophyta humilis during dehydration and rehydration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1WltbjE&md5=81550cfd22072824761238d36c6f6f02CAS |
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research 25, 173–185.
| Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVymsbs%3D&md5=e60f7984bc0f85303de25bf12723a529CAS |
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
| Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7s%3D&md5=c0a3d54246b0668e76fa3410ea5d90a2CAS | 18662937PubMed |
Cheeseman JM (2013) The integration of activity in saline environments: problems and perspectives. Functional Plant Biology 40, 759–774.
Cimato A, Castelli S, Tattini M, Traversi ML (2010) An ecophysiological analysis of salinity tolerance in olive. Environmental and Experimental Botany 68, 214–221.
| An ecophysiological analysis of salinity tolerance in olive.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCmsr0%3D&md5=af1f9a99cdb831dd31a39fa737727eeaCAS |
De Lillis M (1991) An eco-morphological study of the evergreen leaf. Braun-Blanquetia 7, 1–127.
Ding MQ, Hou PC, Shen X, Wang MJ, Deng SR, Sun J, Xiao F, Wang RG, Zhou XY, Lu CF, Zhang D, Zheng X, Hu Z, Chen S (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Molecular Biology 73, 251–269.
| Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFKqsbs%3D&md5=2f6ffe9e209fa0bb45c7661c633f6b61CAS |
Fares S, Mereu S, Scarascia Mugnozza G, Vitale M, Manes F, Frattoni M, Ciccioli P, Gerosa G, Loreto F (2009) The ACCENT-VOCBAS field campaign on biosphere-atmosphere interactions in a Mediterranean ecosystem of Castelporziano (Rome): site characteristics, climatic and meteorological conditions, and eco-physiology of vegetation. Biogeosciences 6, 1043–1058.
| The ACCENT-VOCBAS field campaign on biosphere-atmosphere interactions in a Mediterranean ecosystem of Castelporziano (Rome): site characteristics, climatic and meteorological conditions, and eco-physiology of vegetation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFWjtLrL&md5=af16b4d1bb1f8ddb876fb9ed46d7a560CAS |
Fini A, Guidi L, Ferrini F, Brunetti C, Di Ferdinando M, Biricolti S, Pollastri S, Calamai L, Tattini M (2012) Drought stress has contrasting effects on antioxidant enzymes activity and phenylpropanoid biosynthesis in Fraxinus ornus leaves: an excess light stress affair? Journal of Plant Physiology 169, 929–939.
| Drought stress has contrasting effects on antioxidant enzymes activity and phenylpropanoid biosynthesis in Fraxinus ornus leaves: an excess light stress affair?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFais7k%3D&md5=8a84004c4900498d4c3fd68694abeccfCAS | 22537713PubMed |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqur%2FE&md5=06dcabcbf1411c34a35d7aed78f04afbCAS | 18565144PubMed |
Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where the next? Australian Journal of Plant Physiology 22, 875–884.
| Breeding for salinity resistance in crop plants: where the next?Crossref | GoogleScholarGoogle Scholar |
Flowers TJ, Galal HK, Bromham L (2010) Evolution of halophytes: multiple origins of salt tolerance in land plants. Functional Plant Biology 37, 604–612.
| Evolution of halophytes: multiple origins of salt tolerance in land plants.Crossref | GoogleScholarGoogle Scholar |
García-Plazaola JI, Hernández A, Errasti E, Becerill JM (2002) Occurrence and operation of lutein epoxide cycle in Quercus species. Functional Plant Biology 29, 1075–1080.
| Occurrence and operation of lutein epoxide cycle in Quercus species.Crossref | GoogleScholarGoogle Scholar |
Gratani L, Ghia E (2002) Adaptive strategy at the leaf level of Arbutus unedo L. to cope with Mediterranean climate. Flora 197, 275–284.
| Adaptive strategy at the leaf level of Arbutus unedo L. to cope with Mediterranean climate.Crossref | GoogleScholarGoogle Scholar |
Greaver TL, Sternberg LS (2010) Decreased precipitation exacerbates the effects of sea level on coastal dune ecosystems in open ocean islands. Global Change Biology 16, 1860–1869.
| Decreased precipitation exacerbates the effects of sea level on coastal dune ecosystems in open ocean islands.Crossref | GoogleScholarGoogle Scholar |
Gucci R, Lombardini L, Tattini M (1997) Analysis of leaf water relations of two olive cultivars (Olea europaea L.) differing in tolerance to salinity. Tree Physiology 17, 13–21.
| Analysis of leaf water relations of two olive cultivars (Olea europaea L.) differing in tolerance to salinity.Crossref | GoogleScholarGoogle Scholar | 14759909PubMed |
Guidi L, Degl’innocenti E, Remorini D, Massai R, Tattini M (2008) Interactions of water stress and solar irradiance on the physiology and biochemistry of Ligustrum vulgare. Tree Physiology 28, 873–883.
| Interactions of water stress and solar irradiance on the physiology and biochemistry of Ligustrum vulgare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotFarsbw%3D&md5=4e58912b74c267422037b642aabe66c7CAS | 18381268PubMed |
Havaux M, Dall’Osto L, Cuiné S, Giuliano G, Bassi R (2004) The effect of zeaxanthin as the only xanthophylls on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. Journal of Biological Chemistry 279, 13878–13888.
| The effect of zeaxanthin as the only xanthophylls on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXis1elsbs%3D&md5=32f6e3a45b03b0e7445ad14933e0f00dCAS | 14722117PubMed |
Hernández JA, Belén Aguilar A, Portillo B, López-Gómez E, Beneyto JM, García-Legaz MF (2003) The effect of calcium on the antioxidant enzymes from salt-treated loquat and anger plants. Functional Plant Biology 30, 1127–1137.
| The effect of calcium on the antioxidant enzymes from salt-treated loquat and anger plants.Crossref | GoogleScholarGoogle Scholar |
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica et Biophysica Acta 1817, 182–193.
| The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOgurzM&md5=bec1e17efeeeaa577225f30402a185ffCAS | 21565154PubMed |
Kampfenkel K, Montagu MV, Inzè D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Analytical Biochemistry 225, 165–167.
| Extraction and determination of ascorbate and dehydroascorbate from plant tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjvVahtb0%3D&md5=d3bdbe6ac757dac08db71b5d4da6fce9CAS | 7778771PubMed |
Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiology 20, 131–138.
| Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer.Crossref | GoogleScholarGoogle Scholar | 12651481PubMed |
Martínez-Vilalta J, Mangirón M, Ogaya R, Sauret M, Serrano L, Peñuelas J, Piñol J (2003) Sap flow of three co-occurring Mediterranean woody species under varying atmospheric and soil water conditions. Tree Physiology 23, 747–758.
| Sap flow of three co-occurring Mediterranean woody species under varying atmospheric and soil water conditions.Crossref | GoogleScholarGoogle Scholar | 12839728PubMed |
Mediavilla S, Escudero A (2009) Ontogenetic changes in leaf phenology of two co-occurring Mediterranean oaks differing in leaf life span. Ecological Research 24, 1083–1090.
| Ontogenetic changes in leaf phenology of two co-occurring Mediterranean oaks differing in leaf life span.Crossref | GoogleScholarGoogle Scholar |
Mereu S, Salvatori E, Fusaro L, Gerosa G, Muys B, Manes F (2009) An integrated approach shows different use of water resources from Mediterranean maquis species in a coastal dune ecosystem. Biogeosciences 6, 2599–2610.
| An integrated approach shows different use of water resources from Mediterranean maquis species in a coastal dune ecosystem.Crossref | GoogleScholarGoogle Scholar |
Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
| Non-photochemical quenching. A response to excess light energy.Crossref | GoogleScholarGoogle Scholar | 11299337PubMed |
Munns R (1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant, Cell & Environment 16, 15–24.
| Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1yjsr0%3D&md5=a884c868738a00c05e702ebf444e38dbCAS |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
| Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=0ce1f7aad22c73fffb329d4603f0e836CAS | 18444910PubMed |
Munns R, Passioura JB, Guo J, Chazen O, Cramer GR (2000) Water relations and leaf expansion: importance of time scale. Journal of Experimental Botany 51, 1495–1504.
| Water relations and leaf expansion: importance of time scale.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnt12jur0%3D&md5=b46b6d4713be5893ff016cecaab809d8CAS | 11006301PubMed |
Noreen Z, Ashraf M (2009) Assessment of variation in antioxidative defense system in salt-treated pea (Pisum sativum) cultivars and its putative use as salinity tolerance markers. Journal of Plant Physiology 166, 1764–1774.
| Assessment of variation in antioxidative defense system in salt-treated pea (Pisum sativum) cultivars and its putative use as salinity tolerance markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVSms7zI&md5=5d320f8a4acc03faa0bfb85c95092efaCAS | 19540015PubMed |
Ogaya R, Peñuelas J, Martínez-Vilalta J, Mangirón M (2003) Effects of drought on diameter increment of Quercus ilex, Phillyrea latifolia and Arbutus unedo in a holm oak forest of NE Spain. Forest Ecology and Management 180, 175–184.
| Effects of drought on diameter increment of Quercus ilex, Phillyrea latifolia and Arbutus unedo in a holm oak forest of NE Spain.Crossref | GoogleScholarGoogle Scholar |
Peltzer D, Polle A (2001) Diurnal fluctuations of antioxidative systems in leaves of field grown beech trees (Fagus sylvatica): responses to light and temperature. Physiologia Plantarum 111, 158–164.
| Diurnal fluctuations of antioxidative systems in leaves of field grown beech trees (Fagus sylvatica): responses to light and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtVCqsbg%3D&md5=e621f4a1d5201faec6487e3ddb4b2a6dCAS |
Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat J, Havaux M (2012) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology 158, 1267–1278.
| Chemical quenching of singlet oxygen by carotenoids in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOksb8%3D&md5=97e925a024bed88659308a8ea6972b76CAS | 22234998PubMed |
Schreiber U, Schliva U, Bilger B (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10, 51–62.
| Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXktlGrsbY%3D&md5=67f078f55c77028d8a1620c529206968CAS |
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiologia Plantarum 133, 651–669.
| Potassium transport and plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Oit70%3D&md5=b00298e506b7189fc2da0a5277d6448aCAS | 18724408PubMed |
Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. Journal of Experimental Botany 52, 2207–2211.
Tardieu F, Tuberosa R (2010) Dissection and modelling of abiotic stress tolerance in plants. Current Opinion in Plant Biology 13, 206–212.
| Dissection and modelling of abiotic stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 20097596PubMed |
Tattini M, Gucci R (1999) Ionic relations of Phillyrea latifolia L. plants during NaCl stress and relief from stress. Canadian Journal of Botany 77, 969–975.
Tattini M, Traversi ML (2008) Responses to changes in Ca2+ supply in two Mediterranean evergreens, Phillyrea latifolia and Pistacia lentiscus, during salinity stress and subsequent relief. Annals of Botany 102, 609–622.
| Responses to changes in Ca2+ supply in two Mediterranean evergreens, Phillyrea latifolia and Pistacia lentiscus, during salinity stress and subsequent relief.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12lur3N&md5=8b3d6efc9b5172d1f6026f69100fa2e7CAS | 18701601PubMed |
Tattini M, Gucci R, Coradeschi MA, Ponzio C, Everard JD (1995) Growth, gas exchange and ion content in Olea europaea plants during salinity and subsequent relief. Physiologia Plantarum 95, 203–210.
| Growth, gas exchange and ion content in Olea europaea plants during salinity and subsequent relief.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVSjtA%3D%3D&md5=ebf114ab2395ffdc3346e999def18846CAS |
Tattini M, Gucci R, Romani A, Baldi A, Everard JD (1996) Changes in non-structural carbohydrates in olive (Olea europaea) leaves during root zone salinity stress. Physiologia Plantarum 98, 117–124.
| Changes in non-structural carbohydrates in olive (Olea europaea) leaves during root zone salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvV2ntL0%3D&md5=276e0df5eb468a631ae88ee5c963bbe6CAS |
Tattini M, Montagni G, Traversi ML (2002) Gas exchange, water relations and osmotic adjustment in Phillyrea latifolia grown at various salinity concentrations. Tree Physiology 22, 403–412.
| Gas exchange, water relations and osmotic adjustment in Phillyrea latifolia grown at various salinity concentrations.Crossref | GoogleScholarGoogle Scholar | 11960765PubMed |
Tattini M, Remorini D, Pinelli P, Agati G, Saracini E, Traversi ML, Massai R (2006) Morpho-anatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus. New Phytologist 170, 779–794.
| Morpho-anatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmslSisLs%3D&md5=83bb8833c61c630a90ef15a147151fd1CAS | 16684238PubMed |
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk C, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography 14, 411–421.
| Modulation of leaf economic traits and trait relationships by climate.Crossref | GoogleScholarGoogle Scholar |
Yakir D, Yechiely Y (1995) Plant invasion of newly exposed hypersaline Dead Sea shores. Nature 374, 803–805.
| Plant invasion of newly exposed hypersaline Dead Sea shores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt1Orsrs%3D&md5=2cb117493944241ad5c44007fb8d7e01CAS |
