Photosynthetica 2018, 56(4):1177-1187 | DOI: 10.1007/s11099-018-0810-z

Relationship between photosynthetic rate, water use and leaf structure in desert annual and perennial forbs differing in their growth

L. Gonzalez-Paleo1,*, D.A. Ravetta1
1 Museo Egidio Feruglio, CONICET. Fontana 140, Trelew, Chubut, Argentina

Specific leaf area (SLA) is a key trait to screen plants for ecological performance and productivity; however, the relationship between SLA and photosynthesis is not always up-scalable to growth when comparing multiple species with different life cycles. We explored leaf anatomy in annual and perennial species of Physaria, and related it to photosynthesis and water loss. The annual Physaria gracilis had higher SLA, thinner leaves, and lower investment in protective tissues, than perennial P. mendocina. Physaria angustifolia (annual), and P. pinetorum (perennial) showed intermediate values. Both perennials had a thicker palisade and high photosynthesis, relative to annuals. The larger leaf veins of perennials should allow high water availability to the mesophyll. The thicker palisade should determine high resistance to water flow and help explain their high water-use efficiency. These leaf functions reflect the construction of long-lived leaves that efficiently use resources under environmental limitations of arid environments.

Keywords: leaf anatomy; Physaria; relative growth rate; specific leaf area; total biomass; xylem anatomy

Received: August 9, 2016; Accepted: June 26, 2017; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

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Gonzalez-Paleo, L., & Ravetta, D.A. (2018). Relationship between photosynthetic rate, water use and leaf structure in desert annual and perennial forbs differing in their growth. Photosynthetica, 56(4), 1177-1187. doi: 10.1007/s11099-018-0810-z.
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    References

    1. Aasamaa K., Niinemets U., Sõber A.: Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny-Tree Physiol. 25: 1409-1418, 2005. Go to original source...
    2. Aerts R.: Nutrient resorption from senescing leaves of perennials: Are there general patterns?-J. Ecol. 84: 597-608, 1996. Go to original source...
    3. Alvarez-Clare S., Kitajima K.: Physical defense traits enhance seedling survival of neotropical tree species.-Funct. Ecol. 21: 1044-1054, 2007. Go to original source...
    4. Arbuckle J.L., Wothke W.: AMOS. 4.0 User's Guide. SPSS. Pp. 634. SmallWalters, Chicago 1999
    5. Björkman O.: Response to different quantum flux densities.-In: Lange O.L., Nobel P.S., Osmond C.B., Ziegler H. (ed.): Physiological Plant Ecology I. Response to the Physical Environment. Encyclopedia of Plant Physiology-New Series 12A, Pp. 57-107, Springer-Verlag, Berlin-Heidelberg 1981.
    6. Blum A.: Drought resistance, water-use efficiency, and yield potential-are they compatible, dissonant, or mutually exclusive?-Aust. J. Agric. Res. 56: 1159-1168, 2005. Go to original source...
    7. Brahim K., Ray D.T., Dierig D.A.: Growth and yield characteristics of Lesquerella fendleri as a function of plant density.-Ind. Crops Prod. 9: 63-71, 1998. Go to original source...
    8. Brodribb T.J., Holbrook N.M., Gutiérrez M.V.: Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees.-Plant Cell Environ. 25: 1435-1444, 2002. Go to original source...
    9. Brodribb T.J., Feild T.S., Jordan G.J.: Leaf maximum photosynthetic rate and venation are linked by hydraulics.-Plant Physiol. 144: 1890-1898, 2007.
    10. Castro-Díez P., Puyravaud P., Cornelissen C.: Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types.-Oecologia 124: 476-486, 2000. Go to original source...
    11. Ceccarelli S., Acevedo E., Grando S.: Breeding for yield stability in unpredictable environments: Single traits, interaction between traits, and architecture of genotypes-Euphytica 56: 169-185, 1991. Go to original source...
    12. Dawson J.C., Huggins D.R., Jones S.S.: Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improve the performance of cereal crops in low-input and organic agricultural systems.-Field Crops Res. 107: 89-101, 2008. Go to original source...
    13. de la Riva E.G., Olmo M., Poorter H. et al.: Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 mediterranean woody species along a water availability gradient.-PLoS ONE 11: 1-18, 2016. Go to original source...
    14. Diaz S., Hodgson J.G., Thompson K. et al.: The plant traits that drive ecosystems: Evidence from three continents.-J. Veget. Sci. 15: 295-304, 2004. Go to original source...
    15. Dierig D.A., Thompson A.E., Nakayama F.: Lesquerella commercialization efforts in the United States.-Ind. Crop. Prod. 1: 289-293, 1993.
    16. Enríquez S., Duarte C.M., Sand-Jensen K., Nielsen S.L.: Broadscale comparison of photosynthetic rates across phototrophic organism.-Oecologia 108: 197-206, 1996. Go to original source...
    17. Evans L.T.: Crop Evolution, Adaptation and Yield. Pp. 521. Cambridge Univ. Press, Cambridge 1993.
    18. Evans J.R., Poorter H.: Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain.-Plant Cell Environ. 24: 755-767, 2001. Go to original source...
    19. Ekstein R.L., Karlsson P.S., Weih M.: Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions.-New Phytol. 143: 177-189, 1999. Go to original source...
    20. Field C.B., Mooney H.A.: The photosynthesis-nitrogen relationship in wild plants.-In: Givnish T.J. (ed.): On the Economy of Plant Form and Function. Pp. 25-55. Cambridge University Press, Cambridge, 1986.
    21. Gago J., Douthe C., Florez-Sarasa I. et al.: Opportunities for improving leaf water use efficiency under climate change conditions.-Plant Sci. 226: 108-119, 2014. Go to original source...
    22. Garnier E.: Growth analysis of congeneric annual and perennial grass species.-J. Ecol. 80: 665-675, 1992. Go to original source...
    23. Garnier E., Laurent G.: Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species.-New Phytol. 128: 725-736, 1994. Go to original source...
    24. Garnier E., Cordonnier P., Guillerm J.L., Sonié L.: Specific leaf area and leaf nitrogen concentration in annual and perennial grass species growing in Mediterranean old-fields.-Oecologia 111: 490-498, 1997. Go to original source...
    25. Garnier E., Salager J.L., Laurent G., Sonié L.: Relationships between photosynthesis, nitrogen and leaf structure in 14 grass species and their dependence on the basis of expression-New Phytol. 143: 119-129, 1999. Go to original source...
    26. Garnier E., Laurent G., Bellmann A. et al.: Consistency of species ranking based on functional leaf traits.-New Phytol. 152: 69-83, 2001. Go to original source...
    27. Givnish T.J.: Biomechanical constraints on crown geometry in forest herbs.-In: Givnish T.J. (ed.): On the Economy of Plant Form and Function. Pp. 525-583. Cambridge University Press, Cambridge 1986.
    28. González-Paleo L., Ravetta D.A.: Relationships between reproductive output, morpho-physiological traits and life span in Lesquerella (Brassicaceae)-Ind. Crop. Prod. 34: 1386-1392, 2011a. Go to original source...
    29. González-Paleo L., Ravetta D.A.: Indirect changes associated with a selection program for increased seed-yield in wild species of Lesquerella (Brassicaceae): Are we developing a phenotype opposite to the expected ideotype?-Ind. Crop. Prod. 34: 1372-1380, 2011b. Go to original source...
    30. González-Paleo L., Ravetta D.A.: Carbon acquisition strategies uncoupled from predictions derived from species life-cycle.-Flora 212: 1-9, 2015. Go to original source...
    31. Jackson D.: In situ hybridization in plants.-In: Bowles D.J., Gurr S.J., McPherson M. (ed.): Molecular Plant Pathology: A Practical Approach. Pp. 163-174. Oxford University Press, Oxford 1991.
    32. Jackson L.E., Koch G.W.: The ecophysiology of crops and their wild relatives.-In: Jackson L.E. (ed.): Ecology in Agriculture. Pp. 3-37. Academic Press, San Diego 1997. Go to original source...
    33. Jaikumar N.S., Snapp S.S., Sharkey T.D.: Life history and resource acquisition: Photosynthetic traits in selected accessions of three perennial cereal species compared with annual wheat and rye.-Am. J. Bot. 100: 2468-2477, 2013. Go to original source...
    34. Lambers H., Poorter H.: Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences.-Adv. Ecol. Res. 23: 187-261, 1992. Go to original source...
    35. Lambers H., Poorter H.: Inherent variation in growth rate between higher plants: A search for physiological causes and ecological consequences.-Adv. Ecol. Res. 34: 283-362, 2004. Go to original source...
    36. Long S.P., Zhu X.G., Naidu S.L., Ort D.R.: Can improvement in photosynthesis increase crop yields?-Plant Cell Environ. 29: 315-330, 2006. Go to original source...
    37. Maseda P.H., Fernández R.J.: Stay wet or else: three ways in which plants can adjust hydraulically to their environment.-J. Exp. Bot. 57: 3963-3977, 2006. Go to original source...
    38. Masnatta W.J., Ravetta D.A.: Seed-yield and yield components response to source-sink ratio in annual and perennial species of Lesquerella (Brassicaceae)-Ind. Crop. Prod. 34: 1393-1398, 2011. Go to original source...
    39. Mediavilla S., Escudero A., Heilmeier H.: Internal leaf anatomy and photosynthetic resource-use efficiency: interspecific and intraspecific comparisons.-Tree Physiol. 21: 251-259, 2001. Go to original source...
    40. Meinzer F.C.: Functional convergence in plant responses to the environment.-Oecologia 134: 1-11, 2003 Go to original source...
    41. Meinzer F.C., Goldstein G.: Scaling tip from leaves to whole plants and crumples for photosynthetic gas exchange.-In: Mulkey S.S., Chazdon R.L., Smith A.P. (ed.): Tropical Forest Plant Ecophysiology. Pp. 114-138. Chapman and Hall, New York 1996. Go to original source...
    42. Meziane D., Shipley B.: Interacting determinants of specific leaf area in 22 herbaceous species: effects of irradiance and nutrient availability.-Plant Cell Environ. 22: 447-459, 1999. Go to original source...
    43. Meziane D., Shipley B.: Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply.-Ann. Bot.-London 88: 915-927, 2001. Go to original source...
    44. Nielsen S.L., Enríquez S., Duarte C.M., Sand-Jensen K.: Scaling maximum growth rates across photosynthetic organisms.-Funct. Ecol. 10: 167-175, 1996. Go to original source...
    45. Niinemets Ü.: Components of leaf dry mass per area-thickness and density-alter leaf photosynthetic capacity in reverse directions in woody plants.-New Phytol. 144: 35-47, 1999. Go to original source...
    46. Niinemets Ü.: Is there a species spectrum within the world-wide leaf economics spectrum ? Major variations in leaf functional traits in the Mediterranean sclerophyll Quercus ilex.-New Phytol. 205: 79-96, 2015. Go to original source...
    47. Niklas K.J.: A mechanical perspective on foliage leaf form and function.-New Phytol. 143: 19-31, 1999. Go to original source...
    48. Nobel P.S., Zaragoza L.J., Smith W.K.: Relation between mesophyll surface area, photosynthetic rate and illumination level during development for leaves of Plectranthus parviflorus Henckel.-Plant Physiol. 55: 1067-1070, 1975. Go to original source...
    49. Nobel P.S., Walker D.B.: Structure of leaf photosynthetic tissue.-In: Barber J., Baker N.P.R. (ed.): Photosynthetic Mechanisms and the Environment. Pp. 502-536. Elsevier, London 1985.
    50. Oguchi R., Hikosaka K., Hirose T.: Does the photosynthetic light-acclimation need change in leaf anatomy?-Plant Cell Environ. 26: 505-512, 2003. Go to original source...
    51. Osunkoya O., Bayliss D., Panetta F.D., Vivian-Smith G.: Leaf trait co-ordination in relation to construction cost, carbon gain and resource-use efficiency in exotic invasive and native woody vine species.-Ann. Bot.-London 106: 371-380, 2010. Go to original source...
    52. Pastor-Pastor A., González-Paleo L., Vilela A., Ravetta D.: Agerelated changes in nitrogen resorption and use efficiency in the perennial new crop Physaria mendocina (Brassicaceae)-Ind. Crop. Prod. 65: 227-232, 2015. Go to original source...
    53. Pimentel D., Cerasale D., Stanley R.C. et al.: Annual vs. perennial grain production.-Agr. Ecosyst. Environ. 161: 1-9, 2012. Go to original source...
    54. Ploschuk E.L., Windauer L., Ravetta D.A.: Potential value of traits associated with perennial habit in the development of new oil-seed crops for arid lands. A comparison of Lesquerella fendleri and L. mendocina subjected to water stress.-J. Arid Environ. 47: 373-386, 2001. Go to original source...
    55. Poorter H.: Interspecific variation in relative growth rate: On ecological causes and physiological consequence.-In: Lambers H., Cambridge M.L., Konings H., Pons T.L. (ed.): Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. Pp. 45-68. SPB, The Hague 1989.
    56. Poorter H.: Plant growth and carbon economy.-In: Encyclopedia of Life Sciences. Pp. 14288. Macmillan Publishers Ltd., Nature Publishing, Chischester 2002.
    57. Poorter H., Niinemets Ü., Poorter L. et al.: Causes and consequences of variation in leaf mass per area (LMA): a metaanalysis.-New Phytol. 182: 565-588, 2009. Go to original source...
    58. Ravetta D.A., Soriano A.: Alternatives for the development of new industrial crops for Patagonia.-Ecol. Austral. 8: 297-307, 1998.
    59. Reich P.B., Walters M.B., Ellsworth D.S.: Leaf life-span in relation to leaf, plant and stand characteristics.-Ecol. Monogr. 62: 365-392, 1992. Go to original source...
    60. Reich P.B., Ellsworth D.S., Walters M.B. et al.: Generality of leaf trait relationships: a test across six biomes.-Ecology 80: 1955-1969, 1999. Go to original source...
    61. Sack L., Cowan P.D., Jaikumari N., Holbrook N.M.: The 'hydrology' of leaves: co-ordination of structure and function in temperate woody species.-Plant Cell Environ. 26: 1343-1356, 2003 Go to original source...
    62. Sack L., Frole K.: Leaf structural diversity is related to hydraulic capacity in tropical rainforest trees.-Ecology 87: 483-491, 2006. Go to original source...
    63. Santiago L.S., Goldstein G., Meinzer F.C. et al.: Leaf photosynthetic traits scale with hydraulic conductivity.-Oecologia 140: 543-550, 2004. Go to original source...
    64. Shields L.M.: Leaf xeromorphy as related to physiological and structural influences.-Bot. Rev. 16: 399-447, 1950. Go to original source...
    65. Shipley B.: Cause and Correlation in Biology: A User's Guide to Path Analysis, Structural Equations and Causal Inferences. Pp. 317. Cambridge University Press, Cambridge 2002a.
    66. Shipley B., Vile D., Garnier E. et al.: Functional linkages between leaf traits and net photosynthetic rate: reconciling empirical and mechanistic models.-Funct. Ecol. 19: 602-615, 2005. Go to original source...
    67. Sobrado M.A., Medina E.: General morphology, anatomical structure, and nutrient content of sclerophyllous leaves of "the Bana" vegetation of Amazonas.-Oecologia 45: 341-345, 1980. Go to original source...
    68. Sperry J.S.: Hydraulic constraints on plant gas exchange.-Agr. Forest. Meteorol. 104: 13-23, 2000. Go to original source...
    69. Terashima I., Miyazawa S., Hanba Y.T.: Why are sun leaves thicker than shade leaves?-Consideration based on analyses of CO2, diffusion in the leaf.-J. Plant Res. 114: 93-105, 2001 Go to original source...
    70. Terashima I., Hanba Y.T., Tholen D., Niinemets U.: Leaf functional anatomy in relation to photosynthesis.-Plant Physiol. 155: 108-116, 2011. Go to original source...
    71. Westoby M., Falster D.S., Moles A.T. et al.: Plant ecological strategies: Some leading dimensions of variation between species.-Annu. Rev. Ecol. Syst. 33: 125-159, 2002. Go to original source...
    72. White J.W., Montes R.C.: Variation in parameters related to leaf thickness in common bean (Phaseolus vulgaris L.).-Field Crops Res. 91: 7-21, 2005. Go to original source...
    73. Wright I.J., Cannon K.: Relationships between leaf life span and structural defences in a low-nutrient, sclerophyll flora.-Funct. Ecol. 15: 351-359, 2001. Go to original source...
    74. Wright I.J., Reich P.B., Westoby M. et al.: The worldwide leaf economics spectrum.-Nature 428: 821-827, 2004. Go to original source...
    75. Zhu X.G., Long S.P., Ort D.R.: Improving photosynthetic efficiency for greater yield.-Annu. Rev. Plant Biol. 61: 235-261, 2010. Go to original source...

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