Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Contrasting response mechanisms to root-zone salinity in three co-occurring Mediterranean woody evergreens: a physiological and biochemical study

Massimiliano Tattini A B F , Maria Laura Traversi A , Silvana Castelli C , Stefano Biricolti B , Lucia Guidi D and Rossano Massai E
+ Author Affiliations
- Author Affiliations

A Istituto per la Valorizzazione del Legno e delle Specie Legnose, Consiglio Nazionale delle Ricerche, Via Madonna del Piano 10, I-50019 Sesto F.no, Firenze, Italy.

B Dipartimento di Ortoflorofrutticoltura, Università di Firenze, Viale delle Idee 30, I-50019 Sesto F.no, Firenze, Italy.

C Istituto di Biotecnologie e Biologia Agraria, Consiglio Nazionale delle Ricerche, Via Bassini 15, I-20110 Milano, Italy.

D Dipartimento di Chimica e Biotecnologie Agrarie, Università di Pisa, Via S. Michele degli Scalzi 2, I-56124 Pisa, Italy.

E Dipartimento di Difesa e Coltivazione Specie Legnose, Università di Pisa, Via del Borghetto 80, I-56124 Pisa, Italy.

F Corresponding author. Email: m.tattini@ivalsa.cnr.it

Functional Plant Biology 36(6) 551-563 https://doi.org/10.1071/FP09054
Submitted: 9 March 2009  Accepted: 16 April 2009   Published: 1 June 2009

Abstract

The present study investigated the extent to which physiological and biochemical traits varied because of root-zone salinity in three Mediterranean evergreens differing greatly in their strategies of salt allocation at an organismal level: the ‘salt-excluders’, Olea europaea L. and Phillyrea latifolia L. (both Oleaceae), and Pistacia lentiscus L., which, instead, largely uses Na+ and Cl for osmotic adjustment. Both Oleaceae spp. underwent severe leaf dehydration and reduced net photosynthesis and whole-plant growth to a significantly greater degree than did P. lentiscus. Osmotic adjustment in Oleaceae mostly resulted from soluble carbohydrates, which, in turn, likely feedback regulated net photosynthesis. Salt stress reduced the actual efficiency of PSII photochemistry (ΦPSII) and enhanced the concentration of de-epoxided violaxanthin-cycle pigments in O. europaea and P. latifolia. Phenylpropanoid metabolism was upregulated by salt stress to a markedly greater degree in O. europaea and P. latifolia than in P. lentiscus. In contrast, species-specific variations in leaf lipid peroxidation were not observed in response to salinity stress. The results suggest that the species-specific ability to manage the allocation of potentially toxic ions out of sensitive leaf organs, other than affecting physiological responses, largely determined the extent to which leaf biochemistry, mostly aimed to counter salt-induced oxidative damage, varied in response to salinity stress.

Additional keywords: gas exchange, ionic and water relations, lipid peroxidation, polyphenol metabolism, PSII photochemistry, superoxide dismutase.


References


Agati G, Galardi C, Gravano E, Romani A, Tattini M (2002) Flavonoid distribution in tissues of Phillyrea latifolia leaves as estimated by microspectrofluorometry and multispectral fluorescence microimaging. Photochemistry and Photobiology 76, 350–360.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Agati G, Matteini P, Goti A, Tattini M (2007) Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytologist 174, 77–89.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Babu S, Akhtar TA, Lampi MA, Tripuranthakam S, Dixon GR, Greenberg BM (2003) Similar stress responses are elicited by copper and ultraviolet radiation in the aquatic plant Lemma gibba: implication of reactive oxygen species as common signals. Plant & Cell Physiology 44, 1320–1329.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry 161, 559–566.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Broetto F, Luttge U, Rataiczak R (2002) Influence of light intensity and salt-treatment on mode of photosynthesis and enzymes of the antioxidant response system of Mesembryanthemum crystallinium. Functional Plant Biology 29, 13–23.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chaves MM, Moroco JP, Pereira JS (2003) Understanding plant responses to drought – from genes to the whole plant. Functional Plant Biology 30, 239–264.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Evans RJ, von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiology 110, 339–346.
CAS | PubMed |
open url image1

Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiologia Plantarum 127, 343–352.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell & Environment 31, 602–621.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Flowers TJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Australian Journal of Plant Physiology 22, 875–884.
Crossref | GoogleScholarGoogle Scholar | open url image1

García-Sánchez F, Syvertsen JP, Martinez V, Melgar JC (2006) Salinity tolerance of ‘Valencia’ orange trees on rootstocks with contrasting salt tolerance is not improved by moderate shade. Journal of Experimental Botany 57, 3697–3706.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gucci R, Tattini M (1997) Salinity tolerance in olive. Horticultural Reviews 17, 177–204. open url image1

Gucci R, Lombardini L, Tattini M (1997) Analysis of leaf water relations in leaves of two olive (Olea europaea) cultivars differing in tolerance to salinity. Tree Physiology 17, 13–21.
PubMed |
open url image1

Gucci R , Massai R , Casano S , Gravano E , Lucchesini M (1998) The effect of drought on gas exchange and water potential in leaves of seven Mediterranean woody species. In ‘Impacts of global change on tree physiology and forest ecosystems’. (Eds GMJ Mohren, K Kramer, S Sabaté) pp. 225–231. (Kluwer Academic: Dordrecht)

Guidi L, Degl’Innocenti E, Genovesi S, Soldatini GF (2005) Photosynthetic process and activity of enzymes involved in the phenylpropanoid pathway in resistant and sensitive genotypes of Lycopersicon esculentum L. exposed to ozone. Plant Science 168, 153–160.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
CAS | PubMed |
open url image1

Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences of the United States of America 96, 8762–8767.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Heimler D, Tattini M, Ticci S, Coradeschi MA, Traversi ML (1995) Growth, ion accumulation and lipid composition of two olive genotypes under salinity stress. Journal of Plant Nutrition 18, 1723–1734.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hernández JA, Aguilar AB, Portillo B, Lopez-Gomez E, Beneyto JM, Garcia-Legaz MF (2003) The effect of calcium on the antioxidant enzymes from salt-treated loquat and anger plants. Functional Plant Biology 30, 1127–1137.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive substances assay for estimating lipid peroxidation in plant tissues containing anthocyanins and other interfering compounds. Planta 207, 604–611.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Husain S, von Caemmerer S, Munns R (2004) Control of salt transport from root to shoots of wheat in saline soils. Functional Plant Biology 31, 1115–1126.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kyparissis A, Petropoulou Y, Manetas Y (1995) Summer survival of leaves in a soft-leaved shrub (Phlomis fruticosa L., Labiatae) under Mediterranean field conditions: avoidance of photoinhibitory damage through decreased chlorophyll contents. Journal of Experimental Botany 46, 1825–1831.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kyparissis A, Drilias P, Manetas Y (2000) Seasonal fluctuations in photoprotective (xanthophyll cycle) and photoselective (chlorophylls) capacity in eight Mediterranean plant species belonging to two different growth forms. Australian Journal of Plant Physiology 27, 265–272.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lloyd J, Syvertsen JP, Kriedemann PE (1987) Salinity effects on leaf water relations and gas exchange of ‘Valencia’ orange (Citrus sinensis [L.] Osbeck) on rootstocks with different salt exclusion characteristics. Australian Journal of Plant Physiology 14, 605–617.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loescher WH (1987) Physiology and metabolism of sugar alcohols in higher plants. Physiologia Plantarum 70, 553–557.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Logan BA, Demmig-Adams B, Adams WW, Grace SC (1998) Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field. Journal of Experimental Botany 49, 1869–1879.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Loreto F, Centritto M, Chartzoulakis K (2003) Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant, Cell & Environment 26, 595–601.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lu C, Zhang J (1998) Thermostability of photosystem II is increased in salt-stressed sorghum. Australian Journal of Plant Physiology 25, 317–324.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lu C, Jiang G, Wang B, Zhang J (2003) Salinity treatment shows no effects on photosystem II photochemistry but increases the resistance of photosystem II to heat stress in the halophyte Suaeda salsa. Journal of Experimental Botany 54, 851–860.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Annals of Botany 84, 123–133.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Martinez-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.
CAS | PubMed |
open url image1

Minguez-Mosquera MI, Gandul-Rojas B, Gallardo-Guerrero ML (1992) Rapid method of quantification of chlorophylls and carotenoids in virgin olive oil by high-performance liquid chromatography. Journal of Agricultural and Food Chemistry 40, 60–63.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Müller P, Xiao-Ping L, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Munns R (2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. Journal of Experimental Botany 57, 1025–1043.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52, 1383–1400.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Peguero-Pina JJ, Morales F, Flexas J, Gil-Pelegrin E, Moyas I (2008) Photochemistry, remotely sensed physiological reflectance index and de-epoxidation state of the xanthophyll cycle in Quercus coccifera under intense drought. Oecologia 156, 1–11.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pérez-Pérez JG, Syvertsen JP, Botía P, García-Sánchez F (2007) Leaf water relations and net gas exchange responses of salinized Carrizo citrange seedlings during drought stress and recovery. Annals of Botany 100, 335–345.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pogson BJ, Niyogi KK, Björkman O, DellaPenna D (1998) Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences of the United States of America 95, 13324–13329.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Remorini D, Melgar JC, Guidi L, Degl’Innocenti E, Castelli S, Traversi ML, Massai R, Tattini M (2009) Interaction of root zone salinity and solar irradiance on the physiology and biochemistry of Olea europaea. Environmental and Experimental Botany 65, 210–219.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Romani A, Pineli P, Galardi C, Mulinacci N, Tattini M (2002) Identification and quantification of galloyl derivatives, flavonoid glycosides and anthocyanins in leaves of Pistacia lentiscus L. Phytochemical Analysis 13, 79–86.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Shen B, Jensen RG, Bohnert HJ (1997) Mannitol protects against oxidation by hydroxyl radicals. Plant Physiology 115, 527–532.
CAS | PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Tattini M, Traversi ML (2009) On the mechanism of salt tolerance in olive (Olea europaea L.) under low- or high-Ca2+ supply. Environmental and Experimental Botany 65, 72–81.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tattini M, Gucci R, Coradeschi MA, Ponzio C, Everard JD (1995) Growth, gas exchange and ion content in Olea europaea plants during salinity stress and subsequent relief. Physiologia Plantarum 95, 203–210.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tattini M, Lombardini L, Gucci R (1997) The effect of NaCl stress and relief on gaschange properties of two olive cultivars differing in tolerance to salinity. Plant and Soil 197, 87–93.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
PubMed |
open url image1

Tattini M, Galardi C, Pinelli P, Massai R, Remorini D, Agati G (2004) Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytologist 163, 547–561.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Tattini M, Guidi L, Morassi-Bonzi L, Pinelli P, Remorini D, Degl’Innocenti E, Giordano C, Massai R, Agati G (2005) On the role of flavonoids in the integrated mechanisms of Ligustrum vulgare and Phillyrea latifolia to high solar radiation. New Phytologist 167, 457–470.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Valderrama R, Corpus FJ, Carreras A, Gómez-Rodriguez MV, Chaki M, Pedrajas JR, Fernández-Ocaña A, Del Rio LA, Barroso JP (2006) The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant, Cell & Environment 29, 1449–1459.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wang R, Chen S, Zhou X, Shen X, Deng L , et al. (2008) Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiology 28, 947–957.
CAS | PubMed |
open url image1

Wolf O, Munns R, Tonnett ML, Jeschke WD (1991) The role of the stem in the partitioning of Na+ and K+ in salt-treated barley. Journal of Experimental Botany 42, 697–704.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wynn Jones RG , Storey R , Leigh RA , Ahmad N , Pollard A (1977) A hypothesis on cytoplasmic regulation. In ‘Regulation of cell membranes activities in plants’. (Eds E Marrè, O Ciferri) pp. 159–180. (Elsevier: Amsterdam)

Yakir D, Yechiely Y (1995) Plant invasion of newly exposed hypersaline Dead Sea shores. Nature [Letter] 374, 803–805.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1