Photosynthetic characteristics and light energy conversions under different light environments in five tree species occupying dominant status at different stages of subtropical forest succession
Qiang Zhang A , Tai-Jie Zhang A , Wah Soon Chow B , Xin Xie A , Yuan-Jun Chen A and Chang-Lian Peng A C
+ Author Affiliations
- Author Affiliations
A Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, Key Laboratory of Ecology and Environmental Science in Guangdong Higher Education, College of Life Sciences, South China Normal University, Guangzhou 510631, PR China.
B Division of Plant Science, Research School of Biology, College of Medicine, Biology and Environment, The Australian National University, Canberra, ACT 2601, Australia.
C Corresponding author. Email: pengchl@scib.ac.cn
Functional Plant Biology 42(7) 609-619 https://doi.org/10.1071/FP14355
Submitted: 17 December 2014 Accepted: 8 March 2015 Published: 10 April 2015
Abstract
In order to reveal the mechanism of succession in subtropical forest along a light gradient, we investigated photosynthetic physiological responses to three light environments in five tree species including a pioneer species Pinus massoniana Lamb., two mid-successional species Schima superba Gardn. et Champ. and Castanopsis fissa (Champ. ex Benth.) Rehd. et Wils., and two late-successional species Cryptocarya concinna Hance. and Acmena acuminatissima (BI.) Merr et Perry) that were selected from Dinghu Mountain subtropical forest, South China. Results showed that, among the three kinds of species in all light conditions (100%, 30% and 12% of full sunlight), the pioneer species had the highest photosynthetic capacity (Amax), light saturation point (LSP), carboxylation efficiency (CE) and maximum utilisation rate of triose phosphate (TPU) that characterised a strong photosynthetic capacity and high carbon dioxide uptake efficiency. However, a higher light compensation point (LCP) and dark respiration (Rd) as well as lower apparent quantum yield (AQY) indicated that the pioneer specie cannot adapt to low light conditions. Mid-successional species had photosynthetic characteristics in between pioneer and late-successional species, but had the greatest effective quantum yield of PSII (ΦPSII) and light use efficiency (LUE, expressed in terms of photosynthesis). In contrast to pioneer and mid-successional species, late-successional species had lower photosynthetic capacity and carbon uptake efficiency, but higher shade tolerance and high-light heat dissipation capacity, as characterised by higher levels of total xanthophyll cycle pigments (VAZ) and de-epoxidation state of xanthophyll cycle (DEPs). These results indicate that photosynthetic capacity decreases along the successional axis and that late-successional species have more responsive heat dissipation capability to compensate for their inferior photosynthetic capacity.
Additional keywords: chlorophyll fluorescence, community succession, light intensity, photosynthetic characteristics, photosynthetic control, shade tolerance.
References
Abrams MD, Kubiske ME (1990) Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: influence of light regime and shade-tolerance rank. Forest Ecology and Management 31, 245–253.| Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: influence of light regime and shade-tolerance rank.Crossref | GoogleScholarGoogle Scholar |
Baltzer JL, Thomas SC (2007) Determinants of whole-plant light requirements in Bornean rain forest tree saplings. Journal of Ecology 95, 1208–1221.
| Determinants of whole-plant light requirements in Bornean rain forest tree saplings.Crossref | GoogleScholarGoogle Scholar |
Baroli I, Gutman BL, Ledford HK, Shin JW, Chin BL, Havaux M, Niyogi KK (2004) Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. The Journal of Biological Chemistry 279, 6337–6344.
| Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1Clsbw%3D&md5=7014589ea4b2a84ff551660fa69dd97eCAS | 14665619PubMed |
Barrett SW (1988) Fire suppression’s effects on forest succession within a central Idaho wilderness. Western Journal of Applied Forestry 3, 76–80.
Björkman O, Boardman N, Anderson JM, Thorne S, Goodchild D, Pyliotis N (1972) Effect of light intensity during growth of Atriplex patula on the capacity of photosynthetic reactions, chloroplast components and structure. Carnegie Institution Year Book 71, 115–135.
Cailly AL, Rizza F, Genty B, Harbinson J (1996) Fate of excitation at PSII in leaves, the non-photochemical side. In ‘Abstract book of 10th FESPP Meeting, September 9–13, 1996, Florence, Italy’. Supplement of Plant Physiology and Biochemistry p. 86. (Florence, Italy)
Canham CD, Finzi AC, Pacala SW, Burbank DH (1994) Causes and consequences of resource heterogeneity in forests: interspecific variation in light transmission by canopy trees. Canadian Journal of Forest Research 24, 337–349.
| Causes and consequences of resource heterogeneity in forests: interspecific variation in light transmission by canopy trees.Crossref | GoogleScholarGoogle Scholar |
Coste S, Roggy J-C, Sonnier G, Dreyer E (2010) Similar irradiance-elicited plasticity of leaf traits in saplings of 12 tropical rainforest tree species with highly different leaf mass to area ratio. Functional Plant Biology 37, 342–355.
| Similar irradiance-elicited plasticity of leaf traits in saplings of 12 tropical rainforest tree species with highly different leaf mass to area ratio.Crossref | GoogleScholarGoogle Scholar |
Craine JM, Reich PB (2005) Leaf-level light compensation points in shade-tolerant woody seedlings. New Phytologist 166, 710–713.
| Leaf-level light compensation points in shade-tolerant woody seedlings.Crossref | GoogleScholarGoogle Scholar | 15869634PubMed |
Crone EE, Jones CG (1999) The dynamics of carbon–nutrient balance: effects of cottonwood acclimation to short-and long-term shade on beetle feeding preferences. Journal of Chemical Ecology 25, 635–656.
| The dynamics of carbon–nutrient balance: effects of cottonwood acclimation to short-and long-term shade on beetle feeding preferences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXit1Oit7s%3D&md5=c98428b1049dfed21d552a0fb0af2314CAS |
Ensminger I, Busch F, Huner N (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiologia Plantarum 126, 28–44.
| Photostasis and cold acclimation: sensing low temperature through photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKjtbs%3D&md5=1c3262c75df06e0221eccaf22b2fed75CAS |
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWrt7w%3D&md5=580ad8465ff46edd49bd8f41674c5486CAS | 24306196PubMed |
Favaretto VF, Martinez CA, Soriani HH, Furriel RP (2011) Differential responses of antioxidant enzymes in pioneer and late-successional tropical tree species grown under sun and shade conditions. Environmental and Experimental Botany 70, 20–28.
| Differential responses of antioxidant enzymes in pioneer and late-successional tropical tree species grown under sun and shade conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFOnsbnP&md5=89298bbd51ebe75a897742fa3f726544CAS |
Francisco de Carvalho Gonçalves J, Caranhas de Sousa Barreto D, Moreira dos Santos Jr U, Varmes Fernandes A, de Tarso Barbosa Sampaio P, Silveira Buckeridge M (2005) Growth, photosynthesis and stress indicators in young rosewood plants (Aniba rosaeodora Ducke) under different light intensities. Brazilian Journal of Plant Physiology 17, 325–334.
Selaya GN, Oomen RJ, Netten JJ, Werger MJ, Anten NP (2008) Biomass allocation and leaf life span in relation to light interception by tropical forest plants during the first years of secondary succession. Journal of Ecology 96, 1211–1221.
| Biomass allocation and leaf life span in relation to light interception by tropical forest plants during the first years of secondary succession.Crossref | GoogleScholarGoogle Scholar |
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) – General Subjects 990, 87–92.
| The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=37e580c0b295f017ee0982c6a1b18ceaCAS |
Gilmore AM, Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching. Photosynthesis Research 35, 67–78.
| Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching. Evidence that antheraxanthin explains zeaxanthin-independent quenching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlvF2ku7g%3D&md5=f28511f2ed08bdc7496e4ac7d54c0328CAS | 24318621PubMed |
Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Functional Plant Biology 15, 63–92.
Glitzenstein JS, Harcombe PA, Streng DR (1986) Disturbance, succession, and maintenance of species diversity in an East Texas forest. Ecological Monographs 56, 243–258.
| Disturbance, succession, and maintenance of species diversity in an East Texas forest.Crossref | GoogleScholarGoogle Scholar |
Hall GM, Hollinger DY (2000) Simulating New Zealand forest dynamics with a generalized temperate forest gap model. Ecological Applications 10, 115–130.
| Simulating New Zealand forest dynamics with a generalized temperate forest gap model.Crossref | GoogleScholarGoogle Scholar |
Hallik L, Niinemets Ü, Wright IJ (2009) Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora? New Phytologist 184, 257–274.
| Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Kitb%2FN&md5=6f0f43cebf6f03a6716072430669d361CAS | 19674334PubMed |
Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynthesis Research 82, 73–81.
| A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXntlersr0%3D&md5=89c9851f125ee706748fbc2c2d785303CAS | 16228614PubMed |
Hughes N, Neufeld H, Burkey K (2005) Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata. New Phytologist 168, 575–587.
| Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWgs7%2FI&md5=b2ffd49d552c45491e18a206553bb828CAS | 16313641PubMed |
Ivanov A, Krol M, Maxwell D, Huner N (1995) Abscisic acid induced protection against photoinhibition of PSII correlates with enhanced activity of the xanthophyll cycle. FEBS Letters 371, 61–64.
| Abscisic acid induced protection against photoinhibition of PSII correlates with enhanced activity of the xanthophyll cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFClsbk%3D&md5=81b0d4598dced1489bd6c193344ac65fCAS | 7664885PubMed |
Janse-Ten Klooster SH, Thomas EJP, Sterck FJ (2007) Explaining interspecific differences in sapling growth and shade tolerance in temperate forests. Journal of Ecology 95, 1250–1260.
| Explaining interspecific differences in sapling growth and shade tolerance in temperate forests.Crossref | GoogleScholarGoogle Scholar |
Kitaoka S, Koike T (2005) Seasonal and yearly variations in light use and nitrogen use by seedlings of four deciduous broad-leaved tree species invading larch plantations. Tree Physiology 25, 467–475.
| Seasonal and yearly variations in light use and nitrogen use by seedlings of four deciduous broad-leaved tree species invading larch plantations.Crossref | GoogleScholarGoogle Scholar | 15687095PubMed |
Kobe RK, Pacala SW, Silander JA, Canham CD (1995) Juvenile tree survivorship as a component of shade tolerance. Ecological Applications 5, 517–532.
| Juvenile tree survivorship as a component of shade tolerance.Crossref | GoogleScholarGoogle Scholar |
Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum 86, 180–187.
| Relationship between photosystem II activity and CO2 fixation in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtlSgsbg%3D&md5=deed36d7e6689c8cc4fdd5ad41c78e30CAS |
Liu N, Peng CL, Lin ZF, Lin GZ, Pan XP (2007) Effects of simulated SO2 pollution on subtropical forest succession: toward chlorophyll fluorescence concept. Pakistan Journal of Botany 39, 1921–1935.
Loach K (1967) Shade tolerance in tree seedlings. I. Leaf photosynthesis and respiration in plant raised under artificial shade. New Phytologist 66, 607–621.
| Shade tolerance in tree seedlings. I. Leaf photosynthesis and respiration in plant raised under artificial shade.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXjs1Oktg%3D%3D&md5=85389c6b07b3d962c4e766872601aff2CAS |
Lusk CH (2002) Leaf area accumulation helps juvenile evergreen trees tolerate shade in a temperate rainforest. Oecologia 132, 188–196.
| Leaf area accumulation helps juvenile evergreen trees tolerate shade in a temperate rainforest.Crossref | GoogleScholarGoogle Scholar |
McLaughlin SB, West DC, Shugart HH, Shriner DS (1978) Air pollution effects on forest growth and succession: applications of a mathematical model. In ‘Proceedings of the 71st annual meeting of the air control association’. (Ed. HBH Cooper) pp. 1–16. (Pittsburgh, PA, USA)
Melis A, Spangfort M, Andersson B (1987) Light-absorption and electron-transport balance between photosystem II and photosystem I in spinach chloroplasts. Photochemistry and Photobiology 45, 129–136.
| Light-absorption and electron-transport balance between photosystem II and photosystem I in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhtlGmsrY%3D&md5=d2eb02399e92a55fcab12a6cc2423013CAS |
Montgomery R (2004) Relative importance of photosynthetic physiology and biomass allocation for tree seedling growth across a broad light gradient. Tree Physiology 24, 155–167.
| Relative importance of photosynthetic physiology and biomass allocation for tree seedling growth across a broad light gradient.Crossref | GoogleScholarGoogle Scholar | 14676032PubMed |
Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
| Non-photochemical quenching. A response to excess light energy.Crossref | GoogleScholarGoogle Scholar | 11299337PubMed |
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Biology 50, 333–359.
| Photoprotection revisited: genetic and molecular approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yksbo%3D&md5=d6ede894de92b66a61e9b08c24e78904CAS |
Onoda Y, Saluñga JB, Akutsu K, Aiba S, Yahara T, Anten NP (2014) Trade-off between light interception efficiency and light use efficiency: implications for species coexistence in one-sided light competition. Journal of Ecology 102, 167–175.
| Trade-off between light interception efficiency and light use efficiency: implications for species coexistence in one-sided light competition.Crossref | GoogleScholarGoogle Scholar |
Pacala SW, Canham CD, Saponara J, Silander JA, Kobe RK, Ribbens E (1996) Forest models defined by field measurements: estimation, error analysis and dynamics. Ecological Monographs 66, 1–43.
| Forest models defined by field measurements: estimation, error analysis and dynamics.Crossref | GoogleScholarGoogle Scholar |
Peng S, Wang B (1994) Forest succession of Dinghushan, Guangdong, China. Chinese Journal of Botany 7, 75–80.
Perry LG, Galatowitsch SM (2004) The influence of light availability on competition between Phalaris arundinacea and a native wetland sedge. Plant Ecology 170, 73–81.
| The influence of light availability on competition between Phalaris arundinacea and a native wetland sedge.Crossref | GoogleScholarGoogle Scholar |
Portes M, Damineli D, Ribeiro R, Monteiro J, Souza G (2010) Evidence of higher photosynthetic plasticity in the early successional Guazuma ulmifolia Lam. compared to the late successional Hymenaea courbaril L. grown in contrasting light environments. Brazilian Journal of Biology 70, 75–83.
| Evidence of higher photosynthetic plasticity in the early successional Guazuma ulmifolia Lam. compared to the late successional Hymenaea courbaril L. grown in contrasting light environments.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7osF2mug%3D%3D&md5=b04aa930a44e635ad6f877f04a874eb9CAS |
Reich P, Wright I, Cavender-Bares J, Craine J, Oleksyn J, Westoby M, Walters M (2003) The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164, S143–S164.
| The evolution of plant functional variation: traits, spectra, and strategies.Crossref | GoogleScholarGoogle Scholar |
Sankaran M, Ratnam J, Hanan NP (2004) Tree-grass coexistence in savannas revisited-insights from an examination of assumptions and mechanisms invoked in existing models. Ecology Letters 7, 480–490.
| Tree-grass coexistence in savannas revisited-insights from an examination of assumptions and mechanisms invoked in existing models.Crossref | GoogleScholarGoogle Scholar |
Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In ‘Ecophysiology of photosynthesis’. (Eds ED Schulze, MM Caldwell) pp. 49–70. (Springer-Verlag: Berlin)
Selaya NG, Anten NP (2010) Leaves of pioneer and later-successional trees have similar lifetime carbon gain in tropical secondary forest. Ecology 91, 1102–1113.
| Leaves of pioneer and later-successional trees have similar lifetime carbon gain in tropical secondary forest.Crossref | GoogleScholarGoogle Scholar | 20462124PubMed |
Valentini R, Epron D, de Angelis P, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycles under different levels of water supply. Plant, Cell & Environment 18, 631–640.
| In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycles under different levels of water supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvFKks70%3D&md5=d26c10fe900f461477a348e27f821e2cCAS |
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology Evolution and Systematics 39, 237–257.
| Shade tolerance, a key plant feature of complex nature and consequences.Crossref | GoogleScholarGoogle Scholar |
Veneklaas EJ, Poorter L (1998) Growth and carbon partitioning of tropical tree seedlings in contrasting light environments. In ‘Inherent variation in plant growth: physiological mechanisms and ecological consequences’. (Eds H Lambers, H Poorter, MMI Van Vuuren) pp. 337–361. (Backhuys Publishers: Leiden, The Netherlands)
Walters MB, Reich PB (1999) Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytologist 143, 143–154.
| Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ?Crossref | GoogleScholarGoogle Scholar |
Walters M, Reich P (2000) Trade-offs in low-light CO2 exchange: a component of variation in shade tolerance among cold temperate tree seedlings. Functional Ecology 14, 155–165.
| Trade-offs in low-light CO2 exchange: a component of variation in shade tolerance among cold temperate tree seedlings.Crossref | GoogleScholarGoogle Scholar |
Wen D, Kong G, Lin Z, Ye W (1998) A comparative study on the growth responses to light intensity in seedlings of four subtropical tree species. Journal of Tropical and Subtropical Botany 7, 125–132. [in Chinese with English abstract]
Zar JH (1986) ‘Biostatistician analysis.’ (Prentice Hall: Englewood Cliffs, NJ, USA)
Zhang Q, Chen Y, Song L, Liu N, Sun L, Peng C (2012) Utilization of lightflecks by seedlings of five dominant tree species of different subtropical forest successional stages under low-light growth conditions. Tree Physiology 32, 545–553.
| Utilization of lightflecks by seedlings of five dominant tree species of different subtropical forest successional stages under low-light growth conditions.Crossref | GoogleScholarGoogle Scholar | 22569998PubMed |
