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Anatomical adaptations of the desert species Stipa lagascae against drought stress

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Abstract

Stipa lagascae R. & Sch. (perennial bunchgrass) is one of the most promising steppic species for arid and desert lands of Tunisia. The present study was designed to study the effect of drought on root and leaf anatomy, water relationship, and the growth of three- month-old S. lagascae plants, submitted to water deficit (5, 10, 15, 20, 30 days of withheld irrigation) and grown in pots in greenhouse conditions. The results show that water deficit treatments reduced the biomass accumulation (MS) and leaf water potential (Ψw) of plants. However, leaf relative water content (RWC) decreased significantly only at severe drought. The root’s anatomical features showed reduced root cross-sectional diameter under water deficit. Conversely, epidermis was unaffected by water stress. Moderate and/or severe water deficit (20–30 days) reduced significantly the cortex thickness, cortical cell size, stele diameter, xylem vessel diameter and the stele/root cross-sectional ratio, while the number of cortical cells increased for severe water deficit. The cuticles and mesophyll of S. lagascae was thickened by moderate to severe drought and the entire lamina thickness was increased significantly by 5.8% only after 30 days of water deficit while epidermis was unaffected by water deficit. However, severe water deficit (30 days) decreased the width and the length of the bundle sheath. At the same time, the mesophyll cells size and both the xylem and phloem vessels diameter diminished by 12, 16.8 and 17.5%, respectively. Leaf rolling occurs as a response to water deficit and its level increases as the drought period is progressing in plants while reduced bulliform cells size occurred only at severe water deficit. Our findings suggest a complex network of root and leaf anatomical adaptations such as a reduced vessel size with lesser cortical and mesophyll parenchyma formation and increased leaf rolling. These proprieties are required for the maintenance of water potential and energy storage under water stress which can improve the resistance of S. lagascae to survive in extremely arid areas.

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References

  • Abernethy G.A., Fountain D.W. & Mcmanus M.T. 1998. Observations on the leaf anatomy of Festuca noyaezelandiae and biochemical response to a water deficit. N. Z. J. Bot. 36: 113–123.

    Article  Google Scholar 

  • Akram M. 2011. Growth and yield components of wheat under water stress of different growth stages. Bangl. J. Agril. Res. 36: 455–468.

    Article  Google Scholar 

  • Alvarez J.M., Rocha J.F. & Machado S.R. 2008. Bulliform cells in Loudetiopsis chrysothrix (Nees) Conert and Tristachya leiostachya Nees (Poaceae): Structure in relation to function. Braz. Arch. Biol. Technol. 51: 113–119.

    Article  Google Scholar 

  • Arnold D.H. & Mauseth J.D. 1997. Effetct of environmental factors on developpement of wood. Amer. J. Bot. 86: 367–371.

    Article  Google Scholar 

  • Athar H. & Ashraf M. 2005. Photosynthesis under drought stress, pp. 795-810. In: Pessarakli M. (ed.), Handbook Photosynthesis, second ed. CRC Press, New York, USA.

    Google Scholar 

  • Bacelar E.A., Correia C.M., MoutinhoPereira J.M., Goncalves B.C., Lopes J.I. & TorresPereira J.M. 2004. Sclerophylly and leaf anatomical traits of five fieldgrown olive cultivars growing under drought conditions. Tree Physiol. 24: 233–239.

    Article  PubMed  Google Scholar 

  • Balsamo R.A., Willigen C.V., Bauer A.M. & Farrant J. 2006. Drought tolerance of selected Eragrostis species correlates with leaf tensile properties. Ann. Bot. 97: 985–991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben Ahmed C., Ben Rouina B. & Boukhris M. 2007. Effects of water deficit on olive trees cv. Chemlali under field conditions in arid region in Tunisia. Sci. Hort. 113: 267–277.

    Google Scholar 

  • Bohnert H.J., Nelson D.E. & Jensen R.G. 1995. Adaptations to environmental stresses. Plant Cell 7: 1099–1111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bongi G. & Loreto F. 1989 Gas exchange properties of saltstressed olive (Olea europaea L.) leaves. Plant Physiol. 90: 1408–1416.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosabalidis A.M. & Kofidis G. 2002. Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci. 163: 375–379.

    Article  CAS  Google Scholar 

  • Boughalleb F. & Hajlaoui H. 2011. Physiological and anatomical changes induced by drought in two olive cultivars (cv Zamlati and Chemlali). Acta Physiol. Plant. 33: 53–65.

    Article  Google Scholar 

  • Burghardt M., Burghardt A., Gall J., Rosenberger C. & Riederer M. 2008. Ecophysiological adaptations of water relations of Teucrium, chamaedrys L. to the hot and dry climate of xeric limestone sites in Franconia (Southern Germany). Fiora 203: 3–13.

    Google Scholar 

  • Burnett S.E., Thomas P.A. & Van Iersel M.W. 2000. Postegermination with PEG-8000 reduces growth of Salvia and manigolds. Hortscience 40: 675-679

  • Burnett S.E., Pennisi S.V., Thomas P.A. & van Iersel M.W. 2005. Controlled drought affects morphology and anatomy of Salvia splendens. J. Amer. Soc. Hort. Sci. 130: 775–781.

    Article  Google Scholar 

  • Bussotti F., Bottacci A., Bartolesi A., Grossoni P. & Tani C. 1995. Morphoanatomical alterations in leaves collected from beech trees (Facus sylvatica L.) in conditions of natural water stress. Environ. Exp. Bot. 35: 201–213.

    Article  Google Scholar 

  • Chartzoulakis K., Patakas A. & Bosabalidis A. 1999. Changes in water relations, photosynthesis and leaf anatomy induced by intermittent drought in two olive cultivars. Environ. Exp. Bot. 42: 113–120.

    Article  Google Scholar 

  • Child R.D., Summers J.E., Babij J., Farrent J.W. & Bruce D.M. 2003. Increased resistance to pod chatter is associated with changes in the vascular structure in pods of a resynthesized Brassica napus line. J. Exp. Bot. 54: 1919–1930.

    Article  CAS  PubMed  Google Scholar 

  • Clifford S.C., Arndt S.K., Popp M. & Jones H.G. 2002. Mucilages and polysaccharides in Ziziphus species (Rhamnaceae): localization, composition and physiological roles during drought stress. J. Exp. Bot. 53: 131–138.

    Article  CAS  PubMed  Google Scholar 

  • Cutler D.F., Botha T. & Stevenson D.W. 2007. Plant Anatomy. An applied approach. Blackwell Publishing, Australia.

    Google Scholar 

  • Da Silva S., Castro E.M. & Soares A.M. 2003. Effects of different water regimes on the anatomical characteristics of roots of grasses promising for revegetation of areas surrounding hydroelectric reservoirs. Ciénc Agrotec Lavras 27: 393–397.

    Article  Google Scholar 

  • Dickison W.C. 2000. Integrative Plant Anatomy. Harcourt Academie Press, San Diego, San Francisco, New York, Boston, London, Toronto, Sydney, Tokyo.

    Google Scholar 

  • Domingo R., RuizSánchez M.C., SánchezBlanco M.J. & Torrecillas A. 1999. Water relations, growth and yield of Fino lemon trees under regulated deficit irrigation. Irrig. Sci. 16: 115–123.

    Article  Google Scholar 

  • ElAfry M.M., ElNady M.F. & Abdelmonteleb E.B. 2012. Anatomical studies on droughtstressed wheat plants (TrifÁcum, aestivum L.) treated with some bacterial strains. Acta Biol. Szeg. 56: 165–174.

    Google Scholar 

  • Esau K. 1977. Anatomy of Seed Plants. 2nd ed. New York, John Wiley and Sons, pp. 351–353.

    Google Scholar 

  • Farouk S. & Amany A.R. 2012. Improving growth and yield of cowpea by foliar application of chitosan under water stress. Egy. J. Biol. 14: 14–26.

    Google Scholar 

  • Fini A., Guidib L., Ferrini F., Brunettia C., Di Ferdinandoa M., Biricolti S., Pollastri S., Calamaia L. & Tattini M. 2012. Drought stress has contrasting effects on antioxidant enzymes activity and phenyl propanoid biosynthesis in Fraxinus ornus leaves: An excess light stress affair. J. Plant Physiol. 169: 929–939.

    Article  CAS  PubMed  Google Scholar 

  • Galle A., Haldimann P. & Feller U. 2007. Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytol. 174: 799–810.

    Article  CAS  PubMed  Google Scholar 

  • Gindaba J., Rozanov A. & Negash L. 2004. Response of seedlings of two Eucalyptus and three deciduous tree species from Ethiopia to severe water stress. For. Ecol. Manage. 201: 119–129.

    Article  Google Scholar 

  • Guerfel M., Baccouri O., Boujnah D., Chaibi W. & Zarrouk M. 2009. Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars. Sci. Hortic. 119: 257–263.

    Article  CAS  Google Scholar 

  • Jacobsen A.L., Ewers F.W., Pratt R.B., Paddock W.A. & Davis S.D. 2005. Do xylem fibers affect vessel cavitation resistance. Plant Physiol. 139: 546–556.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James S.A. & Bell D.T. 1995. Morphology and anatomy of leaves of Eucalyptus camaldulensis clones: variation between geographically separated locations. Aust. J. Bot. 43: 415–433.

    Article  Google Scholar 

  • Kadioglu A. & Terzi R. 2007. A dehydration avoidance mechanism: Leaf rolling. Bot. Rev. 73: 290–302.

    Article  Google Scholar 

  • Kamel A. & Loser D.M. 1995. Contribution of carbohydrates and other solutes to osmotic adjustment in wheat leaves under water stress. J. Plant Physiol. 145: 363–366.

    Article  Google Scholar 

  • Kofidis G., Bosabalidis A.M. & Chartzoulakis K. 2004. Leaf anatomical alterations induced by drought stress in two avocado cultivars. J. Biol. Res. 1: 115–120.

    Google Scholar 

  • Kramer J. & Boyer J.S. 1995. Water Relation of Plants and Soils. Elsevier Science (USA), Acad. Press, San Diego, CA, 495 pp.

    Google Scholar 

  • Kutlu N., Terzi R., Tekeli C., Senel G., Battal P. & Kadioglu A. 2009. Changes in anatomical structure and levels of endogenous phytohormones during leaf rolling in Ctenanthe setosa. Turk. J. Biol. 33: 115–122.

    CAS  Google Scholar 

  • Lecoeur J. & Sinclair T.R. 1996. Field pea transpiration and leaf growth in response to soil water de ficits. Crop Sci. 36: 331–335.

    Article  Google Scholar 

  • Le fioch E., Neffati M., Chaieb M., fioret C. & Pontanier R. 1999. Rehabilitation experiment at Menel Habib, Southern Tunisia. Arid Soil Res. Rehab. 13: 357–368.

    Article  Google Scholar 

  • Lersten N.R. & Curtis J.D. 2001. Idioblasts and other unusual internal foliar secretary structures in Scrophulariaceae. Plant Syst. Evol. 227: 63–73.

    Article  Google Scholar 

  • Levitt J. 1972. Responses of Plants to Environmental Stresses. Academie Press, New York, pp. 31–47.

    Google Scholar 

  • Li F.L., Bao W.K. & Wu N. 2011. Morphological, anatomical and physiological responses of Campylotropis polyantha (Francii.) Schindl. seedlings to progressive water stress Sci. Hortic. 127: 436–443.

    Google Scholar 

  • Liu F. & Stiitzel H. 2004. Biomass partitioning, specific leaf area, and water use efficiency of vegetable amaranth (Amaranthus spp.) in response to water stress. Sci. Hortic. 102: 15–27.

    Article  Google Scholar 

  • Lo Gullo M.A., Salleo S., Piaceri E.C. & Rossor. 1995. Relations between vulnerability to xylem embolism and xylem conduit dimensions in young trees of Quercus cerris. Plant Cell Eniviron. 18: 661–669.

    Article  Google Scholar 

  • Lux A., Luxova M., Abe J. & Morita S. 2004. Root cortex: structural and functional variability and responses to environmental stress. Root Res. 13: 117–131.

    Article  Google Scholar 

  • Makbul S., Turkmen Z., Coskuncelebi K. & Beyazoglu O. 2008. Anatomical and pollen characters in the genus Epilobium, L. (Onagraceae) from northeast anatolia. Acta Biol. Cracov. Bot. 50: 57–67.

    Google Scholar 

  • Makbul S., Saruhan G.N., Durmus N. & Guven S. 2011. Changes in anatomical and physiological parameters of soybean under drought stress. Turk. J. Bot. 35: 369–377.

    Google Scholar 

  • Matsuda K. & Rayan A. 1990. Anatomy: A key factor regulating plant tissue response to water stress. In: Kafternan F. (ed.), Environment Injury to Plants, San Diego: Academie Press, 290 pp.

    Google Scholar 

  • Medrano H., Escalona J.M., Bota J., Gulias J. & fiexas J. 2002. Regulation of photosynthesis of C3 plants in response to progressive drought: Stomatal sonductance as a reference parameter. Ann Bot. 89: 895–905.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moulia B. 1994. Biomechanics of leaf rolling. Biomimetics 2: 267–281.

    Google Scholar 

  • Nawazish S., Hameed M. & Naurin S. 2006. Leaf anatomical adaptations of Cenchrus ciliaris L. from the salt range, Pakistan against drought stress. Pak J. Bot. 38: 1723–1730.

    Google Scholar 

  • Nicotra A.B., Babicka N. & Westoby N. 2002. Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130: 136–145.

    Article  CAS  PubMed  Google Scholar 

  • Niu G., Rodriguez D., Mendoza M., Jifon J. & Ganjegunte G. 2012. Reponses of Jatropha curcas to salt and drought stresses. Inter. J. Agronomy. Academie Editor, 7 pp.

    Google Scholar 

  • O’Connor T.G. 1991. Local extinction in perennial grasslands: A lifehistory approach. The Amer. Naturalist 137: 753–773.

    Article  Google Scholar 

  • O’Connor T.G. 1996. Hierarchical control over seedling recruitment of the bunchgrass Themeda triandra in a semiarid savanna. J. App. Ecol. 33: 1094–1106.

    Article  Google Scholar 

  • Ogbonnaya C.I., Nwalozie MC.., RoyMacauley H. & Annerose D. J.M. 1998. Growth and water relations of Kenaf (Hibiscus cannabinus L.) under water deficit on a sandy soil. Ind. Crops Prod. 8: 65–76.

    Article  Google Scholar 

  • Olmos E., SanchezBlanco M.J., Fernandez T. & Alarcon J.J. 2007. Subcellular effects of drought stress in Rosmarinus officinalis. Plant Biol. 9: 77–84.

    Article  CAS  PubMed  Google Scholar 

  • PeńaValdivia C.B., SánchezUrdaneta A.B., Trejo C., Aguirre R.J.R. & Cardenas E. 2005. Root anatomy of drought sensitive and tolerant maize (Zea mays L.) seedlings under different water potentials. Cereal Res. Comm. 33: 705–712.

    Article  Google Scholar 

  • PeńaValdivia C.B. & SánchezUrdaneta A.B. 2009. Effects of substrate water potential in root growth of Agáve salmiana Otto ex SalmDyck seedlings. Biol. Res. 42: 239–248.

    Google Scholar 

  • PeńaValdivia C.B., SánchezUrdaneta A.B., Rangel J.M., Muńoz J.J., GarcíaNava R. & Velázquez R.C. 2010. Anatomical root variations in response to water deficit: wild and domesticated common bean (Phaseolus vulgaris L.) Biol. Res. 43: 417–427.

    Google Scholar 

  • Price A.H., Young E.M. & Tomos A.D. 1997. Quantitative trait loci associated with stomatal conductance, leaf rolling and heading date mapped in upland rice (Oryza sativa). New Phytol. 137: 83–91.

    Article  CAS  Google Scholar 

  • Reddy A.R., Chiatanya K.V. & Vivekanandan M. 2004. Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. J. Plant Physiol. 161: 1189–1202.

    Article  CAS  Google Scholar 

  • Rosales M., CuellarOrtiz S., AcostaGallegos J. & Cavarrabias A. 2012. Physiological traits related to terminal drought resistance in common bean Phaseolus vulgaris L. J. Sci. Food Agric. 93: 324–331.

    Article  PubMed  CAS  Google Scholar 

  • Sairam R.K. & Tyagi A. 2004. Physiology and molecular biology of salinity stress tolerance in plants. Curr. Sci. 6: 407–421.

    Article  Google Scholar 

  • Saleem M., Lamkemeyer T., Schutzenmeister M.T., Sakai H., Piepho H.P., Nordheim A. & Hochholdinge F. 2010. Speci fication of cortical parenchyma and stele of maize primary roots by asymmetric levels of auxin, cytokinin, and cytokininregulated proteins. Plant Physiol. 152: 4–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salisbury F.B. & Ross C.W. 1992. Plant Physiology. Wadsworth Publishing Company, Belmont.

    Google Scholar 

  • Sam O., Jeréz E. & Varela M. 1996. Caracteristicas anatomicas de hojas de apa (Solanum, tuberosum L.) y tomate (Lycopersycon esculentum Mill.) can diferentes grados de tolerancia a estres de humedad y temperatura. Cultivos Tropicales 17: 32–38.

    Google Scholar 

  • Sam O., Jeréz E., Dell’Amico J. & RuizSánchez M.C. 2000. Water stress induced changes in anatomy of tomato leaf epidermis. Biol. Plant. 43: 275–277.

    Article  Google Scholar 

  • Scholz H. 1991. Stipa tunetana, eine neue Artaus Tunesien, und das St. lagascae Aggregat (Gramineae). Willdenowia 26: 225–228.

    Google Scholar 

  • Schultz H.R. & Matthews M.A. 1988. Resistance to water transport in shoots of VifÁs vinifero, L. Plant Physiol. 88: 718–724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Selim H. & ElNady M. 2011. Physioanatomical responses of drought stressed tomato plants to magnetic field. Acta Astro. 2: 1–9.

    Google Scholar 

  • Shao H.B., Chu L.Y., Jaleel CA. & Zhao C.X. 2008. Water deficit stress induced anatomical changes in higher plants. C. R. Biol. 331: 215–225.

    Article  PubMed  Google Scholar 

  • Shilei G., Sheng Z. & Hong W. 2002. Anatomical characters of stems and leaves of three lawn grasses. J. Trop. Subtrop. Bot. 10: 145–151.

    Google Scholar 

  • Sibounheuang V., Basnayake J. & Fukai S. 2006. Genotypic consistency in the expression of leaf water potential in rice (Oryzo, sativa L.). Field Crops Res. 97: 142–154.

    Article  Google Scholar 

  • Silva S., Soares A.M., Oliveira L.E.M. & Magalháes P.C. 2001. Respostas fisiológicas de gramíneas promissoras para revegetação ciliar de reservatórios hidrelétricos, submetidas à deficięncia hídrica. Cięncia Agrotécnica 25: 124–133.

    Google Scholar 

  • Singh A., Shamim M. & Singh K.N. 2013. Genotypic variation in root anatomy, starch accumulation, and protein induction in upland rice (Oryzo, sativa) varieties under water stress. Agric. Res. 2: 24–30.

    Article  CAS  Google Scholar 

  • Srivastava L.M. 2001. Plant growth and development. Digital stock Inc., 718 pp.

    Google Scholar 

  • Stiller V., Lafitte H.R. & Sperry J.S. 2003. Hydraulic properties of rice and the response of gas exchange to water stress. Plant Physiol. 132: 1698–1706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stolf R., Medri M.E., Pimenta J.A., Boeger M.R.T., Dias J., Lemos N.G., de Oliveira M.C.N., Brogin R.L., Yamanaka N., Neumaier N., Farias J.R.B. & Nepomuceno A.L. 2009. Morphoanatomical and micromorphometrical evaluations in soybean genotypes during water stress. Braz. Arch Biol. Technol. 52: 1313–1331.

    Article  Google Scholar 

  • Syvertsen J.F., Lloyd J., McConchie C., Kriedemann P.E. & Farquhar G.D. 1995. On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ. 18: 149–157.

    Article  Google Scholar 

  • Twumasi P., van Ieperen W., Woltering E.J., Emons A.M.C., Schel J.H.N., Schel J.F.H., van Meeteren U. & van Marwijk D. 2005. Effects of water stress during growth on xylem anatomy, xylem functioning and vaše life in three Zinnia elegans cultivars. Acta Hort. 669: 303–311.

    Article  Google Scholar 

  • Uga Y., Okuno K. & Yano M. 2008. QTLs underlying natural variation in stele and xylem structures of rice root. Breeding Sci. 58: 7–14.

    Article  CAS  Google Scholar 

  • van Ieperen W., Nijsse J., Keijzer C.J. & Van Meeteren U. 2001. Induction of air embolism in xylem conduits of prede fined diameter. J. Exp. Bot. 52: 981–991.

    Article  PubMed  Google Scholar 

  • Vasellati V., Oesterheld M., Medan D. & Loreti J. 2001. Effects of flooding and drought on the anatomy of Paspalum, dilatatum. Ann. Bot. 88: 355–360.

    Article  Google Scholar 

  • Wang W., Vincour B. & Altman A. 2003. Plant responses to drought, salinity and extréme temperatures: towards genetic engineering for stress tolerance. Planta 218: 1–14.

    Article  CAS  PubMed  Google Scholar 

  • Xiang J.J., Zhang G.H., Qian Q. & HongWei X.H.W. 2012. Encodes a putative glycosylphosphatidylinositolanchored protein and modulates rice leaf rolling by regulating the formation of bulliform cells. Plant Physiol. 159: 1488–1500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann M.H. 1983. Xylem Structure and the Ascent of Sap. SpringerVerlag, Berlin, Heidelberg, New York, Tokyo, 143 pp.

    Book  Google Scholar 

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We gratefully acknowledge all the technical staff of the Arid Regions Institute-Medenine (IRA) for their help to conductingthese experiments.

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Boughalleb, F., Abdellaoui, R., Hadded, Z. et al. Anatomical adaptations of the desert species Stipa lagascae against drought stress. Biologia 70, 1042–1052 (2015). https://doi.org/10.1515/biolog-2015-0125

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