Skip to main content
Log in

Sex-related differences in leaf traits in an androdioecious shrub under contrasting levels of soil salinity

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

This study explores whether male and hermaphrodite plants of Phillyrea angustifolia (Oleaceae) show physiological and structural differences at the leaf level under severe water stress driven by drought and soil salinity. Leaf traits were measured in summer, at the height of the summer drought period, in male and hermaphrodite plants from two adjacent sites under contrasting soil salinity levels. Male plants from the saline site had significantly higher leaf proline content compared to males from the nonsaline site. By contrast, leaf proline levels were similarly low in hermaphrodite plants from both sites. On the other hand, hermaphrodite plants from the saline site had higher leaf stomatal frequency than hermaphrodites from the nonsaline site, whereas this parameter did not differ for male plants across sites. Such differences could be interpreted as the result of two different solutions to the same selective pressure in the androdioecious shrub P. angustifolia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ain-Lhout F, Zunzunegui M, Diaz-Barradas MC, Tirado R, Clavijo A, García-Novo F (2001) Comparison of proline accumulation in two Mediterranean shrubs subjected to natural and experimental water deficit. Plant Soil 230:175–183

    Article  CAS  Google Scholar 

  • Al-Shahib W, Marshall RJ (2003) The fruit of the date palm: its possible use as the best food for the future? Int J Food Sci Nutr 54:247–259

    Article  PubMed  Google Scholar 

  • Bassett PA (1978) The vegetation of a Camargue pasture. J Ecol 66:803–827

    Article  Google Scholar 

  • Bates LS, Waldren RB, Teare ED (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beerling DJ, Heath J, Woodward FI, Mansfield TA (1996) Drought–CO2 interactions in trees: observations and mechanisms. New Phytol 134:235–242

    Article  Google Scholar 

  • Case AL, Ashman T-L (2005) Sex-specific physiology and its implications for the cost of reproduction. In: Reekie E, Bazzazz F (eds) Reproductive allocation in plants. Elsevier Science, London, pp 126–154

    Google Scholar 

  • Chaerle L, Saibo N, Van Der Straeden D (2005) Tuning the pores: towards engineering plants for improved water use efficiency. Trends Biotechnol 23:308–315

    Article  PubMed  CAS  Google Scholar 

  • Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    Article  PubMed  CAS  Google Scholar 

  • Cherubini P, Gartner BL, Tognetti R, Bräcker OU, Schoch W, Innes JL (2003) Identification, measurement and interpretation of tree rings in woody species from Mediterranean climates. Biol Rev 78:119–148

    Article  PubMed  Google Scholar 

  • Cottenie K, De Meester L (2003) Comment to Oksanen (2001): reconciling Oksanen (2001) and Hurlbert (1984). Oikos 100:394–396

    Article  Google Scholar 

  • Dawson TE, Geber MA (1999) Sexual dimorphism in physiology and morphology. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, pp 175–215

    Google Scholar 

  • Duhme F, Hinckley TM (1992) Daily and seasonal variation in water relations of macchia shrubs and trees in France (Montpellier) and Turkey (Antalya). Vegetatio 100:185–198

    Article  Google Scholar 

  • Ferris R, Long L, Bunn SM, Robinson KM, Bradshaw HD, Rae AM, Taylor G (2002) Leaf stomatal and epidermal cell development: identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar. Tree Physiol 22:633–640

    PubMed  CAS  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189

    Article  PubMed  CAS  Google Scholar 

  • Gratani L, Varone L (2004) Adaptive photosynthetic strategies of the Mediterranean maquis species according to their origin. Photosynthetica 42:551–558

    Article  Google Scholar 

  • Gravano E, Tani C, Bennici A, Gucci R (1998) The ultrastructure of glandular trichomes of Phillyrea latifolia L. (Oleaceae) leaves. Ann Bot 81:327–335

    Article  Google Scholar 

  • Gucci R, Aronne G, Lombardini L, Tattini M (1997) Salinity tolerance in Phillyrea species. New Phytol 135:227–234

    Article  CAS  Google Scholar 

  • Guitián J (1995) Sex ratio, reproductive investment and flowering phenology in dioecious Rhamnus alaternus (Rhamnaceae). Nord J Bot 15:139–143

    Article  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation in plants. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Hlwatika CNM, Bhat RB (2002) An ecological interpretation of the difference in leaf anatomy and its plasticity in contrasting tree species in Orange Kloof, Table Mountain, South Africa. Ann Bot 89:109–114

    Article  PubMed  CAS  Google Scholar 

  • Hsieh TH, Lee JT, Charng YY, Chan MT (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130:618–626

    Article  PubMed  CAS  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Article  Google Scholar 

  • Hurlbert SH (2004) On misinterpretations of pseudoreplication and related issues: a reply to Oksanen. Oikos 104:591–597

    Article  Google Scholar 

  • Izhaki I (1993) Influence of nonprotein nitrogen on estimation of protein from total nitrogen in fleshy fruits. J Chem Ecol 19:2605–2615

    Article  CAS  Google Scholar 

  • Kalapos T (1994) Leaf water potential–leaf water deficit relationship for ten species of a semiarid grassland community. Plant Soil 160:105–112

    Article  Google Scholar 

  • Kapotis G, Zervoudakis G, Veltsistas T, Salahas G (2003) Comparison of chlorophyll meter readings with leaf chlorophyll concentration in Amaranthus vlitus: correlation with physiological processes. Russ J Plant Physiol 50:395–397

    Article  CAS  Google Scholar 

  • Kavi-Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci India 88:424–438

    Google Scholar 

  • Kloeppel BD, Abrams MD (1995) Ecophysiological attributes of the native Acer saccharum and the exotic Acer platanoides in urban oak forests in Pennsylvania, USA. Tree Physiol 15:739–746

    PubMed  Google Scholar 

  • Kozlowski TT, Pallardy SG (1997) Physiology of woody plants. Academic, New York, p 411

    Google Scholar 

  • Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic, San Diego, p 495

    Google Scholar 

  • Lange OL, Tenhunen JD, Braun M (1982) Midday stomatal closure in Mediterranean-type sclerophylls under simulated habitat conditions in an environmentally controlled chamber. Flora 172:563–579

    Google Scholar 

  • Meagher TR (1984) Sexual dimorphism and ecological differentiation of male and female plants. Ann Mo Bot Gard 71:254–264

    Article  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  PubMed  CAS  Google Scholar 

  • Nardini A, Lo Gullo MA, Salleo S (1999) Competitive strategies for water availability in two Mediterranean Quercus species. Plant Cell Environ 22:109–116

    Article  Google Scholar 

  • Nicotra AB (1999) Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a tropical dioecious shrub. J Ecol 13:138–149

    Article  Google Scholar 

  • Nicotra AB, Chazdon RL, Montgomery RA (2003) Sexes show contrasting patterns of leaf and crown carbon gain in a dioecious rainforest shrub. Am J Bot 90:347–355

    Article  Google Scholar 

  • Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348

    Article  Google Scholar 

  • Oksanen L (2001) Logic of experiments in ecology: is ‘pseudoreplication’ a pseudoissue? Oikos 94:27–28

    Article  Google Scholar 

  • Oksanen L (2004) The devil lies in details: reply to Stuart Hurlbert. Oikos 104:598–605

    Article  Google Scholar 

  • Orshan G, Floret C, Le Floch E, Le Roux A, Montenegro G, Romane F (1989) General synthesis. In: Orsham G (ed) Plant pheno-morphological studies in Mediterranean-type ecosystems. Kluwer Academic, Dordrecht, pp 389–399

    Google Scholar 

  • Pannell JR (2002) The evolution and maintenance of androdioecy. Annu Rev Ecol Evol Syst 33:397–425

    Article  Google Scholar 

  • Pannell JR, Ojeda F (2000) Patterns of flowering and variation in the sex ratio of the Mediterranean shrub Phillyrea angustifolia (Oleaceae): implications for the maintenance of males with hermaphrodites. Ecol Lett 3:495–592

    Article  Google Scholar 

  • Pérez-Latorre AV, Cabezudo B (2002) Use of monocharacteristic growth forms and phenological phases to describe and differentiate plant communities in Mediterranean-type ecosystems. Plant Ecol 161:231–249

    Article  Google Scholar 

  • Raven JA (1985) Regulation of pH and generation of osmolarity in vascular plants: a cost–benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytol 101:25–77

    Article  CAS  Google Scholar 

  • Rejšková A, Patková L, Stodůlková E, Lipavská H (2007) The effect of abiotic stresses on carbohydrate status of olive shoots (Olea europaea L.) under in vitro conditions. J Plant Physiol 164:174–184

    Article  PubMed  CAS  Google Scholar 

  • Rotondi A, Rossi F, Asunis C, Cesaraccio C (2003) Leaf xeromorphic adaptations of some plants of a coastal Mediterranean macchia ecosystem. J Medit Ecol 4:25–35

    Google Scholar 

  • Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Palaeobot Palyno 114:1–28

    Article  Google Scholar 

  • Sofo A, Dichio B, Xiloyannis C, Masia A (2004) Lipoxygenase activity and proline accumulation in leaves and roots of olive trees in response to drought stress. Physiol Plantarum 121:58–65

    Article  CAS  Google Scholar 

  • Stines AP, Naylor DJ, Høj PB, van Heeswijck R (1999) Proline accumulation in developing grapevine fruit occurs independently of changes in the levels of Δ1-pyrroline-5-carboxylate synthetase mRNA or protein. Plant Physiol 120:923–931

    Article  PubMed  CAS  Google Scholar 

  • Tenhunen JD, Catarino FM, Lange OL, Oechel WC (1987) Plant response to stress. Functional analysis in Mediterranean ecosystems. NATO ASI series. Springer, Berlin, p 668

    Google Scholar 

  • Traveset A (1994) Reproductive biology of Phillyrea angustifolia L. (Oleaceae) and effect of galling-insects on its reproductive output. Bot J Linn Soc 114:153–166

    Google Scholar 

  • Vassiliadis C, Saumitou-Laprade P, Lepart J, Viard F (2002) High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia. Evolution 56:1362–1373

    PubMed  CAS  Google Scholar 

  • Whitney DA (1998) Soil salinity. In: Brown JR (ed) Recommended chemical soil test procedures for the North Central Region. Missouri Agricultural Experiment Station SB 1001, Columbia, pp 59–60

    Google Scholar 

  • Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Francisco Bravo, director of Bahía de Cádiz Natural Park, for kindly providing facilities for field work; Ana Cruz for helping with leaf proline measurements, and Fernando Ramírez-Pousa and Antonio Nieto for helping with leaf glandular trichome and stomata counting; and Miguel Verdú, Roberto Salguero, John Pannell, and Juan Arroyo for providing useful comments on the manuscript. This study was funded by research projects BOS2002-00609 and AGL2005-07440-C02-02/FOR from the Spanish Ministerio de Educación y Ciencia, and by a FPI-MEC scholarship to JLMG.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Ojeda.

Additional information

Responsible Editor: Tibor Kalapos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Medina-Gavilán, J.L., Bartual, A. & Ojeda, F. Sex-related differences in leaf traits in an androdioecious shrub under contrasting levels of soil salinity. Plant Soil 310, 235–243 (2008). https://doi.org/10.1007/s11104-008-9653-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-008-9653-x

Keywords

Navigation