Foliar plasticity related to gradients of heat and drought stress across crown orientations in three Mediterranean Quercus species
Autoři:
Sonia Mediavilla aff001; Ignacio Martín aff002; Josefa Babiano aff002; Alfonso Escudero aff001
Působiště autorů:
Área de Ecología, Facultad de Biología, Universidad de Salamanca, Campus Miguel de Unamuno, Salamanca, Spain
aff001; Dpto. de Botánica y Fisiología Vegetal, Facultad de Biología, Universidad de Salamanca, Campus Miguel de Unamuno, Salamanca, Spain
aff002
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224462
Souhrn
Studies on plasticity at the level of a single individual plant provide indispensable information to predict leaf responses to climate change, because they allow better identification of the environmental factors that determine differences in leaf traits in the absence of genetic differences. Most of these studies have focused on the responses of leaf traits to variations in the light environment along vertical gradients, thus paying less attention to possible differences in the intensity of water stress among canopy orientations. In this paper, we analyzed the differences in leaf traits traditionally associated with changes in the intensity of water stress between east and west crown orientations in three Quercus species. The leaves facing west experienced similar solar radiation levels but higher maximum temperatures and lower daily minimum water potentials than those of the east orientation. In response to these differences, the leaves of the west orientation showed smaller size and less chlorophyll concentration, higher percentage of palisade tissue and higher density of stomata and trichomes. These responses would confirm the role of such traits in the tolerance to water stress and control of water losses by transpiration. For all traits, the species with the longest leaf life span exhibited the greatest plasticity between orientations. By contrast, no differences between canopy positions were observed for leaf thickness, leaf mass per unit area and venation patterns.
Klíčová slova:
Leaves – Stomata – Photosynthesis – Trees – Density – Chlorophyll – Trichomes – Leaf veins
Zdroje
1. Garnier E, Shipley B, Roumet C, Laurent G. A standardized protocol for the determination of specific leaf area and leaf dry matter content. Funct Ecol. 2001; 15: 688–695.
2. Roche P, Diaz-Burlinson N, Gachet S. Congruency analysis of species ranking based on leaf traits: which traits are the more reliable? Plant Ecol. 2004; 174: 37–48.
3. de la Riva EG, Olmo M, Poorter H, Ubera JL, Villar R. Leaf mass per area (LMA) and its relationship with leaf structure and anatomy in 34 Mediterranean woody species along a water availability gradient. PlosOne 2016; 11(2): e0148788.
4. Guo CH, Ma L, Yuan S, Wang R. Morphological, physiological and anatomical traits of plant functional types in temperate grasslands along a large-scale aridity gradient in northeastern China. Sci Rep. 2017; 7: 40900. doi: 10.1038/srep40900 28106080
5. Matesanz S, Gianoli E, Valladares F. Global change and the evolution of phenotypic plasticity in plants. Ann N Y Acad Sci. 2010; 1206: 35–55. doi: 10.1111/j.1749-6632.2010.05704.x 20860682
6. Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 2010; 15: 684–692. doi: 10.1016/j.tplants.2010.09.008 20970368
7. Gratani L. Plant Phenotypic Plasticity in Response to Environmental Factors. Adv Bot. 2014; Article ID 208747.
8. Herrera CM, Medrano M, Bazaga P. Continuous within-plant variation as a source of intraspecific functional diversity: patterns, magnitude, and genetic correlates of leaf variability in Helleborus foetidus (Ranunculaceae). Am J Bot. 2015; 102: 225–232. doi: 10.3732/ajb.1400437 25667075
9. Messier J, McGill BJ, Enquist BJ, Lechowicz MJ. Trait variation and integration across scales: is the leaf economic spectrum present at local scales? Ecography 2017; 40: 685–697.
10. Sack L, Melcher PJ, Wendy HL, Middleton E, Pardee T. How strong is intracanopy leaf plasticity in temperate deciduous trees? Am J Bot. 2006; 93: 829–839. doi: 10.3732/ajb.93.6.829 21642145
11. Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A et al. A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol Lett. 2015; 18: 1406–1419. doi: 10.1111/ele.12508 26415616
12. Escribano-Rocafort AG, Ventre-Lespiaucq AB, Granado-Yela C, Rubio R, Delgado JA, Escudero A et al. Intraindividual variation in light-related functional traits: magnitude and structure of leaf trait variability across global scales in Olea europaea trees. Trees 2017; 31: 1505–1517.
13. Manze U. Die Nervaturdichte der Blätter als Hilfsmittel der Paläoklimatologie. University Köln, Sonderveröff Geol Inst. 1968; 14:103S.
14. Díaz-Espejo A, Nicolás E, Fernández JE. Seasonal evolution of diffusional limitations and photosynthetic capacity in olive under drought. Plant Cell Environ. 2007; 30: 922–933. doi: 10.1111/j.1365-3040.2007.001686.x 17617820
15. Escudero A, Fernández J, Cordero A, Mediavilla S. Distribution of leaf characteristics in relation to orientation within the canopy of woody species. Acta Oecol. 2013; 48: 13–2.
16. Flexas J, Medrano H. Photosynthetic responses of C3 plants to drought. In: Hemantaranjan A, editor. Advances in Plant Physiology IV. Scientific Publishers, Jodhpur, India; 2002. pp. 1–56.
17. Leight A, Sevanto S, Close JD, Nicotra AB. The influence of leaf size and shape on leaf thermal dynamics: does theory hold up under natural conditions? Plant Cell Environ. 2017; 70: 237–248.
18. Scoffoni C, Rawls M, McKown A, Cochard H, Sack L. Decline of leaf hydraulic conductance with dehydration: Relationship to leaf size and venation architecture. Plant Physiol. 2011; 156: 832–843. doi: 10.1104/pp.111.173856 21511989
19. Agrawal AA, Fishbein M, Jetter R, Salminen JP, Goldstein JB, Freitag AE et al. Phylogenetic ecology of leaf surface traits in the milkweeds (Asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol. 2009; 183: 848–867. doi: 10.1111/j.1469-8137.2009.02897.x 19522840
20. Kenzo T, Yoneda R, Azani MA, Majid NM. Changes in leaf water use after removal of leaf lower surface hairs on Mallotus macrostachyus (Euphorbiaceae) in a tropical secondary forest in Malaysia. J For Res. 2008; 13: 137–142.
21. Mediavilla S, Escudero A. Photosynthetic capacity, integrated over the lifetime of a leaf, is predicted to be independent of leaf longevity in some tree species. New Phytol. 2003; 159: 203–211.
22. Dorronsoro F. El medio físico-químico: suelos. In: Gómez-Gutiérrez JM, editor El Libro de las Dehesas Salmantinas. Junta de Castilla y León, Salamanca, España; 1992. pp. 71–124.
23. Abràmoff M, Magalhães P, Ram S. Image processing with ImageJ. Biophotonics Intern. 2004; 11: 36–42.
24. Peguero-Pina JJ, Sisó S, Sancho-Knapik D, Díaz-Espejo A, Flexas J, Galmés J et al. Leaf morphological and physiological adaptations of a deciduous oak (Quercus faginea Lam.) to the Mediterranean climate: a comparison with a closely related temperate species (Quercus robur L.). Tree Physiol 2016; 36: 287–299. doi: 10.1093/treephys/tpv107 26496958
25. Molinas ML. The stomata of the cork‐oak, Quercus suber. An ultrastructural approach. Nord J Bot 1991; 11: 205–212.
26. Loreto F, Cicioli P, Cecinato A, Brancaleoni E, Frattoni M, Tricoli D. Influence of environmental factors and air composition on the emission of [alpha]-pinene from Quercus ilex leaves. Plant Physiol 1996; 110: 267–275. doi: 10.1104/pp.110.1.267 12226182
27. Maherali H, Reid CD, Polley HW, Johnson HB, Jachson RB. Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant Cell Environ. 2002; 25: 557–566.
28. Bourland FM, Hornbeck JM. Variation in marginal bract trichome density in upland cotton. J Cotton Sci. 2007; 11: 242–251.
29. Whatley FR, Arnon DI. Photosynthetic phosphorylation in plants. In: Colowick SP, Kaplan NO, editors. Methods in enzymology VI. Academic Press, New York; 1963. pp. 308–313.
30. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72: 248–254. doi: 10.1006/abio.1976.9999 942051
31. Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW. Plastic phenotypic response to light of 16 rainforests shrubs (Psychotria) differing in shade tolerance. Ecology 2000; 81: 1925–1936.
32. López R, Climent J, Gil L. Intraspecific variation and plasticity in growth and foliar morphology along a climate gradient in the Canary Island pine. Trees 2010; 24: 343–350.
33. Franks PJ, Beerling DJ. Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl AcadSci USA. 2009; 106: 10343–10347.
34. Lin H, Chen Y, Zhang H, Fu P, Fan Z. Stronger cooling effects of transpiration and leaf physical traits of plants from a hot dry habitat than from a hot wet habitat. Funct Ecol. 2017; 31: 2202–2211.
35. Xu Z, Zhou G. Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot. 2008; 59: 3317–3325. doi: 10.1093/jxb/ern185 18648104
36. Doheny-Adams T, Hunt L, Franks PJ, Beerling DJ, Gray JE. Genetic manipulation of stomatal density influences stomatal size, plant growth and tolerance to restricted water supply across a growth carbon dioxide gradient. PhilosTrans Royal Soc.B 2012; 367: 547–555.
37. Fraser LH, Greenall A, Carlyle C, Turkington R, Friedman CR. Adaptive phenotypic plasticity of Pseudoroegnerias picata: response of stomatal density, leaf area and biomass to changes in water supply and increased temperature. Ann Bot. 2009; 103: 769–775. doi: 10.1093/aob/mcn252 19088084
38. Werker E. Trichome diversity and development. Adv Bot Res. 2000; 31: 1–35.
39. Karabourniotis G, Bornman J. Penetration of UV-A, UV-B and blue light through the leaf trichome layers of two xeromorphic plants, olive and oak, measured by optical fibre microprobes. Physiol Plant. 1999; 105: 655–661.
40. Ehleringer J, Cook C. Characteristics of Encelia species differing in leaf reflectance and transpiration rate under common garden conditions. Oecologia 1990; 82: 484–489. doi: 10.1007/BF00319790 28311472
41. Bongi G, Palliotti A. Olive. In: Schaffe B, Andersen PC, editors. Handbook of environmental physiology of fruit crops. Vol. I Temperature Crops. CRC Press Inc., Boca Raton Florida USA; 1994. pp. 165–187.
42. Wang R, Huang W, Chen L, Ma L, Gua C, Liu X. Anatomical and physiological plasticity in Leymus chinensis (Poaceae) along large-scale longitudinal gradient in northeast China. PLoSOne 2011; 6 (11): e26209.
43. Wright IJ, Reich PB, Cornelissen JH, Falster DS, Groom PK, Hikosaka K, et al. Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr. 2005; 14: 411–421.
44. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, et al. The worldwide leaf economics spectrum. Nature 2004; 428: 821–827. doi: 10.1038/nature02403 15103368
45. Reich PB. The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol. 2014; 102: 275–301.
46. Turner IM. Sclerophylly: primarily protective? Funct Ecol. 1994; 8: 669–675.
47. Niinemets Ü. Global- scale climatic controls of leaf dry mass per area, density and thickness in trees and shrubs. Ecology 2001; 82: 453–469.
48. González- Zurdo P, Escudero A, Babiano J, García-Ciudad A, Mediavilla S. Costs of leaf reinforcement in response to winter cold in evergreen species. Tree Physiol.2016; 36: 273–286. doi: 10.1093/treephys/tpv134 26764268
49. Witkowski ETF, Lamont BB. Leaf specific mass confounds leaf density and thickness. Oecologia 1991; 88: 486–493. doi: 10.1007/BF00317710 28312617
50. Bacelar EA, Santos DL, Moutinho-Pereira JM, Gonçalves BC, Ferreira HF, Correia CM. Immediate responses and adaptative strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci. 2004; 170: 596–605.
51. Guerfel M, Baccouri O, Boujnah D, Chaibi W, Zarrouk M. Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars. SciHortic. 2009; 119: 257–263.
52. Krober W, Heklau H, Bruelheide H. Leaf morphology of 40 evergreen and deciduous broadleaved subtropical tree species and relationships to functional ecophysiological traits. Plant Biol. 2015; 17: 373–383. doi: 10.1111/plb.12250 25441614
53. Gil-Pelegrín E, Saz MA, Cuadrat JM, Peguero-Pina JJ & Sancho-Knapik D. Oaks under Mediterranean–type climates: functional response to summer aridity. In: Gil Pelegrín E, Peguero Pina JJ, Sancho-Knapik D, editors. Oaks Physiological ecology. Exploring the functional diversity of genus Quercus L. Tree Physiology 7. Springer International Publishing AG 2917, pp 137–194.
54. Wei H, Luo T, Wu B. Optimal balance of water use efficiency and leaf construction cost with a link to the drought threshold of the desert steppe ecotone in northern China. Ann Bot. 2016; 118: 541–553. doi: 10.1093/aob/mcw127 27443298
55. Sack L, Frole K. Leaf structural diversity is related to hydraulic capacity in tropical rainforest trees. Ecology 2006; 87: 483–491. doi: 10.1890/05-0710 16637372
56. Zwieniecki MA, Brodribb TJ, Holbrook NM. Hydraulic design of leaves: insights from rehydration kinetics. Plant Cell Environ. 2007; 30: 910–921. doi: 10.1111/j.1365-3040.2007.001681.x 17617819
57. Sack L, Scoffoni C, McKown AD, Frole K, Rawls M, Havran JC et al. Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nat Commun. 2012; 3: 1–10.
58. Nardini A, Peda G, La Rocca N. 2012. Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytol. 2012; 196: 788–798. doi: 10.1111/j.1469-8137.2012.04294.x 22978628
59. Uhl D, Mosbrugger V. Leaf venation density as a climate environmental proxy: a critical review and new data. Palaeogeogr Palaeoclimatol Palaeoecol 1999; 149: 15–26.
60. Dunbar-Co S, Sporck MJ, Sack L. Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. Int J Plant Sci. 2009; 170: 61–75.
61. Zhu Y, Kang H, Xie Q, Wang Z, Yin S, Liu C. Pattern of leaf vein density and climate relationship of Quercus variabilis populations remains unchanged with environmental changes. Trees 2012; 26:597–607.
62. Hikosaka K, Anten NPR, Borjigidai A, Kimiyama C, Sakai H, Hasegawa T et al. A meta-analysis of leaf nitrogen distribution within plant canopies. Ann Bot. 2016; 118: 239–247. doi: 10.1093/aob/mcw099 27296134
63. Kyparissis A, Petropoulou Y, Manetas Y. 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. J Exp Bot 1995; 46: 1825–1831.
64. Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbo M. Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physio Plant. 2006; 127: 343–352.
65. Yang J, Cao M, Swenson NG. Why functional traits do not predict tree demographic rates. Trends Ecol Evol 2018; 33: 326–336. doi: 10.1016/j.tree.2018.03.003 29605086
66. Mediavilla S, Escudero A. Ontogenetic changes in leaf phenology of two co-occurring Mediterranean oaks differing in leaf life span. Ecol. Res. 2009; 24: 1083–1090.
67. Mediavilla S, Herranz M, González-Zurdo P, Escudero A. Ontogenetic transition in leaf traits: a new cost associated with the increase in leaf longevity. J Plant Ecol.2014; 7: 567–575.
68. Niinemets U, Díaz-Espejo A, Flexas J, Galmés J, Warren CR. Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. J Exp Bot. 2006; 60: 2249–2270.
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