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Specific leaf area variations drive acclimation of Cistus salvifolius in different light environments

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Photosynthetica

Abstract

Cistus salvifolius L. is the most widely spread Cistus species around the Mediterranean basin. It colonizes a wide range of habitats growing from sea level to 1,800 m a.s.l., on silicolous and calcicolous soils, in sun areas as well as in the understory of wooded areas. Nevertheless, this species has been mainly investigated in term of its responsiveness to drought. Our aim was to understand which leaf traits allow C. salvifolius to cope with low-light environments. We questioned if biochemical and physiological leaf trait variations in response to a reduced photosynthetic photon flux density were related to leaf morphological plasticity, expressed by variations of specific leaf area (SLA) and its anatomical components (leaf tissue density and thickness). C. salvifolius shrubs growing along the Latium coast (41°43'N,12°18'E, 14 m a.s.l., Italy) in the open and in the understory of a Pinus pinea forest, were selected and the relationships between anatomical, gas exchange, chlorophyll (Chl) fluorescence, and biochemical parameters with SLA and PPFD variations were tested. The obtained results suggested long-term acclimation of the selected shrubs to contrasting light environments. In high-light conditions, leaf nitrogen and Chl contents per leaf area unit, leaf thickness, and Chl a/b ratio increased, thus maximizing net photosynthesis, while in shade photosynthesis, it was downregulated by a significant reduction in the electron transport rate. Nevertheless, the increased pigment-protein complexes and the decreased Chl a/b in shade drove to an increased light-harvesting capacity (i.e. higher actual quantum efficiency of PSII). Moreover, the measured vitality index highlighted the photosynthetic acclimation of C. salvifolius to contrasting light environments. Overall, our results demonstrated the morphological, anatomical, and physiological acclimation of C. salvifolius to a reduced light environment.

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Abbreviations

C/N:

ratio between soil organic carbon content and total soil nitrogen content

C a :

CO2 concentration in the leaf chamber

Cab :

abaxial cuticle thickness

Cad :

adaxial cuticle thickness

Car:

carotenoids

Car/Chl:

ratio between Car and Chl (a+b)

C e :

apparent carboxylation efficiency

Chl:

chlorophyll

C i :

intercellular CO2 concentration

DM:

dry mass

E :

transpiration rate

ETab :

abaxial epidermis thickness

ETad :

adaxial epidermis thickness

ETR:

electron transport rate

f ias :

fraction of the mesophyll occupied by intercellular air spaces

FM:

fresh mass

Fm :

maximal fluorescence yield of the dark-adapted state

Fm':

maximal fluorescence yield of the light-adapted state

Fs :

steady-state fluorescence yield

g s :

stomatal conductance

LA:

leaf area

LMA:

leaf mass area

LT:

total leaf thickness

LTD:

leaf tissue density

Narea :

nitrogen content per unit leaf area

Nleaf :

leaf nitrogen content

NORG :

organic nitrogen content per unit of leaf area

NP :

nitrogen allocated to the pigment-protein complexes

NP% :

NP as percentage of NORG

P:

palisade parenchyma thickness

P N :

net photosynthetic rate

R/FR:

ratio between irradiance in the red and far red wavelengths

R D :

respiration rate

R D/P N :

ratio between R D and P N

Rfd :

vitality index

S:

spongy parenchyma thickness

SD:

stomatal density

SLA:

specific leaf area

SPA:

stomatal pore area

SPL:

stomatal pore length

SPW:

stomatal pore width

Tl:

leaf temperature

T m :

mean air temperature

T max :

mean maximum air temperature

T min :

mean minimum air temperature

WUEi :

intrinsic water-use efficiency

a:

absorptance

ΦFPSII:

effective quantum yield of PSII photochemistry

χ:

chlorophyll content per unit of leaf area

References

  • Atkin O.K., Evans J.R., Siebke K.: Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment. - Aust. J. Plant. Physiol. 25: 437–443, 1998.

    Article  Google Scholar 

  • Attaguile G., Russo A., Campisi A. et al.: Antioxidant activity and protective effect on DNA cleavage of extracts from Cistus incanus L. and Cistus monspeliensis L. - Cell. Biol. Toxicol. 16: 83–90, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Bartolini S., Minnocci A., Vitagliano C.: Influence of temperature on morphoanatomic characteristics of “Trebbiano” gravepine leaves. - Agricolt. Mediterr. 127: 37–43, 1997.

    Google Scholar 

  • Bosch J.: Floral biology and pollinators of three co-occurring Cistus species (Cistaceae). - Bot. J. Linn. Soc. 109: 39–55, 1992.

    Article  Google Scholar 

  • Cai Z., Slot M., Fan Z.: Leaf development and photosynthetic properties of three tropical tree species with delayed greening. - Photosynthetica 43: 91–98, 2005.

    Article  CAS  Google Scholar 

  • Chabot B.F., Chabot J.F.: Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. - Oecologia 26: 363–377, 1977.

    Article  Google Scholar 

  • Delgado-Sánchez P., Yáñez-Espinosa L., Jiménez-Bremont J.F. et al.: Ecophysiological and anatomical mechanisms behind the nurse effect: Which are more important? A multivariate approach for cactus seedlings. - PLoS ONE 8: e81513, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  • DellaPenna D., Pogson B.J.: Vitamin synthesis in plants: tocopherols and carotenoids. - Annu. Rev. Plant. Biol. 57: 711–738, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Evans J.R.: Photosynthesis and nitrogen relationships in leaves of C3 plants. - Oecologia 78: 9–19, 1989.

    Article  Google Scholar 

  • Evans J.R.: Leaf anatomy enables more equal access to light and CO2 between chloroplasts. - New Phytol. 143: 93–104, 1999.

    Article  Google Scholar 

  • Evans J.R., Poorter H.: Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf areamand nitrogen partitioning in maximizing carbon gain. - Plant Cell Environ. 24: 755–767, 2001.

    Article  CAS  Google Scholar 

  • Farley R.A., McNeilly T.: Diversity and divergence in Cistus salvifolius (L.) populations from contrasting habitats. - Hereditas 132: 183–192, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Mazuecos M., Vargas P.: Ecological rather than geographical isolation dominates Quaternary formation of Mediterranean Cistus species. - Mol. Ecol. 19: 1381–1395, 2010.

    Article  PubMed  Google Scholar 

  • Flexas J., Gulías J., Jonasson S. et al.: Seasonal patterns and control of gas exchange in local populations of the Mediterranean evergreen shrub Pistacia lentiscus L. - Acta Oecol. 22: 33–43, 2001.

    Article  Google Scholar 

  • Galmés J., Flexas J., Savé R., Medrano H.: Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. - Plant Soil 290: 139–155, 2007.

    Article  Google Scholar 

  • Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - Biochim. Biophys. Acta 990: 87–92, 1989.

    Article  CAS  Google Scholar 

  • Grant O.M., Tronina Ł., García-Plazaola J.I. et al.: Resilience of a semi-deciduous shrub, Cistus salvifolius, to severe summer drought and heat stress. - Funct. Plant Biol. 42: 219–228, 2014.

    Article  Google Scholar 

  • Gratani L.: Plant phenotypic plasticity in response to environmental factors. - Adv. Bot. 2014: 208–747, 2014.

    Google Scholar 

  • Guzmán B., Lledó M.D., Vargas P.: Adaptive radiation in Mediterranean Cistus. - PLoS ONE 4: 1–13, 2009.

    Article  Google Scholar 

  • Hallik L., Niinemets Ü., Kull O.: Photosynthetic acclimation to light in woody and herbaceous species: a comparison of leaf structure, pigment content and chlorophyll fluorescence characteristics measured in the field. - Plant Biol. 14: 88–99, 2012.

    CAS  PubMed  Google Scholar 

  • Harley P.C., Tenhunen J.D., Beyschlag W., Lange O.L.: Seasonal changes in net photosynthesis rates and photosynthetic capacity in leaves of Cistus salvifolius, a European Mediterranean semideciduous shrub. - Oecologia 74: 380–388, 1987.

    Article  Google Scholar 

  • Holm G.: Chlorophyll mutations in barley. - Acta Agr. Scand. BS P. 4: 457–471, 1954.

    Article  Google Scholar 

  • Kitajima K., Hogan K.P.: Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. - Plant Cell Environ. 26: 857–865, 2003.

    Article  PubMed  Google Scholar 

  • Krall J.P., Edwards G.E.: Relationship between photosystem IIactivity and CO2 fixation in leaves. - Physiol. Plantarum 86: 180–187, 1992.

    Article  CAS  Google Scholar 

  • Kull O., Niinemets Ü.: Variation in leaf morphometry and nitrogen concentration in Betula pendula Roth., Corylus avellana L. and Lonicera xylosteum L. - Tree Physiol. 12: 311–318, 1993.

    Article  CAS  PubMed  Google Scholar 

  • Kursar T.A.: Relating tree physiology to past and future changes in tropical rainforest tree communities. - Climatic Change 39: 363–379, 1998.

    Article  Google Scholar 

  • Lichtenthaler H.K., Rinderle U.: The role of chlorophyll fluorescence in detection of stress conditions in plants. - Crit. Rev. Anal. Chem. 19: S29–S85, 1988.

    Article  Google Scholar 

  • MacLachlan S., Zalik S.: Plastid structure, chlorophyll concentration, and free aminoacid composition of a chlorophyll mutant of barley. - Can. J. Bot. 41: 1053–1062, 1963.

    Article  CAS  Google Scholar 

  • Matsubara S., Krause G.H., Aranda J. et al.: Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. - Funct. Plant. Biol. 36: 20–36, 2009.

    Article  CAS  Google Scholar 

  • Mendes M.M., Gazarini L.C., Rodrigues M.L.: Acclimation of Myrtus communis to contrasting Mediterranean light environments–effects on structure and chemical composition of foliage and plant water relations. - Environ. Exp. Bot. 45: 165–178, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Middleton L.: Shade-tolerant flowering plants: adaptations and horticultural implications. - Acta Hortic. 552: 95–102, 2001.

    Article  Google Scholar 

  • Mishra M.K.: Stomatal characteristics at different ploidy levels in Coffea L. - Ann. Bot.-London 80: 689–692, 1997.

    Article  Google Scholar 

  • Nar H., Saglam A., Terzi R. et al.: Leaf rolling and photosystem IIefficiency in Ctenanthe setosa exposed to drought stress. - Photosynthetica 47: 429–436, 2009.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Niinemets Ü.: The controversy over traits conferring shadetolerance in trees: ontogenetic changes revisited. - J. Ecol. 94: 464–470, 2006.

    Article  Google Scholar 

  • Niinemets Ü.: Photosynthesis and resource distribution through plant canopies. - Plant Cell Environ. 30: 1052–1071, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Niinemets Ü.: A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. - Ecol. Res. 25: 693–714, 2010.

    Article  Google Scholar 

  • Niinemets Ü., Kull O.: Stoichiometry of foliar carbon constituents varies along light gradients in temperate woody canopies: implications for foliage morphological plasticity. - Tree Physiol. 18: 467–479, 1998.

    Article  PubMed  Google Scholar 

  • Niinemets Ü., Kull O., Tenhunen J.D.: Within canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. - Plant Cell Environ. 27: 293–313, 2004.

    Article  CAS  Google Scholar 

  • Núñez-Olivera E., Martínez-Abaigar J., Escudero J.C.: Adaptability of leaves of Cistus ladanifer to widely varying environmental conditions. - Funct. Ecol. 10: 636–646, 1996.

    Article  Google Scholar 

  • Papaefthimiou D., Papanikolaou A., Falara V. et al.: Genus Cistus: a model for exploring labdane- type-diterpenes’ biosynthesis and a natural source of high value products with biological, aromatic, and pharmacological properties. - Front. Chem. 2: 1–19, 2014.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Price T.D., Qvarnström A., Irwin D.E.: The role of phenotypic plasticity in driving genetic evolution. - P. Roy. Soc. Lond. B Bio. 270: 1433–1440, 2003.

    Article  Google Scholar 

  • Puglielli G., Crescente M.F., Frattaroli A.R., Gratani L.: Morphological, anatomical and physiological leaf trait plasticity of Sesleria nitida in open vs shaded conditions. - Pol. J. Ecol. 63: 10–22, 2015.

    Article  Google Scholar 

  • Reich P.B., Walters M.B., Kloeppel B.D., Ellsworth D.S., Walters M.B.: Different photosynthesis nitrogen relations in deciduous hardwood and evergreen coniferous tree species. - Oecologia 104: 24–30, 1995.

    Article  Google Scholar 

  • Sack L., Cowan P.D., Jaikumar 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.

    Article  Google Scholar 

  • Sack L., Melcher P.J., Liu W.H. et al.: How strong is intracanopy leaf plasticity in temperate deciduous trees? - Am. J. Bot. 93: 829–839, 2006.

    Article  PubMed  Google Scholar 

  • Short M.J.: Cistaceae. - In: Press J.R., Short M.J. (ed.): Flora of Madeira. Pp. 226–227. The Natural History Museum, HMSO, London 1994.

    Google Scholar 

  • Syvertsen J.P., Lloyd J., McConchie C. et al.: On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. - Plant Cell Environ. 18: 149–157, 1995.

    Article  Google Scholar 

  • Valladares F., Niinemets Ü.: Shade tolerance, a key plant feature of complex nature and consequences. - Annu. Rev. Ecol. Evol. S. 39: 237–257, 2008.

    Article  Google Scholar 

  • Warburg E.F.: Cistus L. - In: Tutin T.G., Heywood V.H., Burges N.A. et al. (ed.): Flora Europaea, Vol. 2. Pp.282–285. Cambridge University Press, Cambridge 1968.

    Google Scholar 

  • Wright I.J., Westoby M.: Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. - New Phytol. 155: 403–416, 2002.

    Article  Google Scholar 

  • Yamashita N., Koike N., Ishida A.: Leaf ontogenetic dependence of light acclimation in invasive and native subtropical trees of different successional status. - Plant Cell Environ. 25: 1341–1356, 2002.

    Article  Google Scholar 

  • Yang S., Sun M., Zhang Y. et al.: Strong leaf morphological, anatomical, and physiological responses of a subtropical woody bamboo (Sinarundinaria nitida) to contrasting light environments. - Plant Ecol. 215: 97–109, 2014.

    Article  Google Scholar 

  • Zunzunegui M., Ain-Lhout F., Díaz Barradas M.C. et al.: Physiological, morphological and allocation plasticity of a semi-deciduous shrub. - Acta Oecol. 35: 370–379, 2009.

    Article  Google Scholar 

  • Zunzunegui M., Díaz-Barradas M.C., Jáuregui J. et al.: Seasondependent and independent responses of Mediterranean scrub to light conditions. - Plant Physiol. Bioch. 102: 80–91, 2016.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Environmental Biology, Sapienza University of Rome, P.le A. Moro 5, 00185, Rome, Italy

    G. Puglielli, L. Varone, L. Gratani & R. Catoni

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  1. G. Puglielli
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  2. L. Varone
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  3. L. Gratani
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  4. R. Catoni
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Correspondence to G. Puglielli.

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Puglielli, G., Varone, L., Gratani, L. et al. Specific leaf area variations drive acclimation of Cistus salvifolius in different light environments. Photosynthetica 55, 31–40 (2017). https://doi.org/10.1007/s11099-016-0235-5

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  • DOI: https://doi.org/10.1007/s11099-016-0235-5

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