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Steady-state and dynamic photosynthetic performance and nitrogen partitioning in the shade-demanding plant Panax notoginseng under different levels of growth irradiance

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Abstract

In this study, we examined steady-state and dynamic photosynthetic performance and leaf nitrogen (N) partitioning in the typical shade-demanding herb Panax notoginseng grown along a light gradient. Gas exchange on a leaf area basis was significantly reduced under low irradiance, with gas exchange on a leaf mass basis reaching a maximum value and then decreasing along the light gradient. Specific leaf area significantly increased with decreasing irradiance levels (P < 0.001), whereas carboxylation efficiency was decreased (P < 0.001). In addition, decreasing growth irradiance levels led to declines in maximum carboxylation rate (V cmax) and maximum electron transport rate (J max), although V cmax/mass and J max/mass were relatively less affected than V cmax/area and J max/area. Slow photosynthetic response to simulated sunflecks was observed under low levels of growth irradiance, with stomatal limitations only detected in leaves grown under low-light conditions. Chlorophyll content increased significantly with decreasing irradiance levels. N content on a leaf mass basis apparently increased, while N content on a leaf area basis markedly decreased. The fraction of leaf N allocated to light-harvesting components increased significantly with decreasing growth irradiance levels, whereas the fraction allocated to carboxylation and bioenergetics was significantly reduced. As an adaptation strategy to growth irradiance, we conclude that adjustments in specific leaf area may be more important than changes in leaf physiology and biochemistry in typical shade-demanding species such as P. notoginseng.

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Abbreviations

PFD:

Photon flux density

N:

Nitrogen

AQY:

Apparent quantum yield

R d :

Dark respiration rate

LCP:

Light compensation point

iWUE:

Intrinsic Water use efficiency

g s-max :

Maximum stomatal conductance

A max :

Maximum net photosynthetic assimilation rate

A net :

Net photosynthetic assimilation rate

P C :

Fraction of leaf N allocated to carboxylation in g g−1

P B :

Fraction of leaf N allocated to bioenergetics in g g−1

P L :

Fraction of leaf N allocated to light-harvesting components in g g−1

A′max :

Light- and CO2-saturated A net

V cmax :

Maximum carboxylation rate

J max :

Maximum electron transport rate

SLA:

Specific leaf area

References

  • Agyeman VK, Swaine MD, Thompson J (1999) Responses of tropical forest seedlings to irradiance and the derivation of a light response index. J Ecol 87:815–827

    Article  Google Scholar 

  • Allen MT, Pearcy RW (2000a) Stomatal versus biochemical limitation to dynamic photosynthetic photosynthetic performance in four tropical rainforest shrub species. Oecologia 122:479–486

    Article  Google Scholar 

  • Allen MT, Pearcy RW (2000b) Stomatal behavior and photosynthetic performance under dynamic light regimes in a seasonally dry tropical rain forest. Oecologia 122:470–478

    Article  Google Scholar 

  • Anten NPR (1997) Modeling canopy photosynthesis using parameters determined from simple non-destructive measurements. Ecol Res 12:77–88

    Article  Google Scholar 

  • Bai KD, Liao DB, Jiang DB, Cao KF (2008) Photosynthetic induction in leaves of co-occuring Fagus Iucida and Castanopsis lamontii saplings grown in contrasting light environments. Trees 22:449–462

    Article  CAS  Google Scholar 

  • Bazzaz FA, Carlson RW (1982) Photosynthetic acclimation to variability in the light environment of early and late successional plants. Oecologia 54:313–316

    Article  Google Scholar 

  • Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259

    Article  CAS  Google Scholar 

  • Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of Plant Physiology. Springer-Verlag, New York, pp 57–107

    Google Scholar 

  • Bond BJ, Farnsworth BT, Coulombe RA, Winner WE (1999) Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance. Oecologia 120:183–192

    Article  Google Scholar 

  • Chazdon RL (1992) Photosynthetic plasticity of two rain forest shrubs across natural gap transects. Oecologia 92:586–595

    Article  Google Scholar 

  • Chazdon RL, Pearcy RW, Lee DW, Fetcher N (1996) Photosynthetic response of tropical forest plants to contrasting light environments. In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Chapman and Hall, New York, pp 5–55

    Chapter  Google Scholar 

  • Chen JW, Zhang Q, Li XS, Cao KF (2011) Steady and dynamic photosynthetic responses of seedlings from contrasting successional groups under low-light grown conditions. Physiol Plant 141:84–95

    Article  CAS  PubMed  Google Scholar 

  • Davies SJ (1998) Photosynthesis of nine pioneer Macaranga species from Borneo in relation to life history. Ecology 79:2292–2308

    Article  Google Scholar 

  • Denslow JS (1987) Tropical rainforest gaps and tree species diversity. Annu Rev Ecol Syst 18:431–451

    Article  Google Scholar 

  • Evans JR (1989a) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Evans JR (1989b) Partitioning of nitrogen between and within leaves grown under different irradiances. Aust J Plant Physiol 16:533–548

    Google Scholar 

  • Evans JR (1998) Photosynthetic characteristics of fast- and slow growing species. In: Lambers H, Poorter H, Van Vuuren MMI (eds) Inherent variation in plant growth. Backhuys Publishers, Leiden, The Netherlands, Physiological Mechanisms and Ecological Consequences, pp 183–198

    Google Scholar 

  • Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning. Plant Cell Environ 24:755–767

    Article  CAS  Google Scholar 

  • Feng YL, Auge H, Ebeling SK (2007) Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153:501–510

    Article  PubMed  Google Scholar 

  • Frak E, Le Roux X, Millard P, Dreyer E, Jaouen G, Saint-Joanis B, Wendler R (2001) Changes in total leaf nitrogen and partitioning of leaf nitrogen drive photosynthetic acclimation to light in fully developed walnut leaves. Plant Cell Environ 24:1279–1288

    Article  CAS  Google Scholar 

  • Garnier E, Salager J-L, Laurent G, Sonié L (1999) Relationships between photosynthesis, nitrogen and leaf structure in 14 grass species and their dependence on the basis of expression. New Phytol 143:119–129

    Article  Google Scholar 

  • Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92

    Google Scholar 

  • Gratani L, Covone F, Larcher W (2005) Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis. Trees 20:549–558

    Article  Google Scholar 

  • Griffin JJ, Ranney TG, Pharr DM (2004) Photosynthesis, chlorophyll fluorescence, and carbohydrate content of IIIicium taxa grown under varied irradiance. J Am Soc Hort Sci 129:46–53

    Google Scholar 

  • Hallik L, Niinemets Ü, Kull O (2012) 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

    CAS  PubMed  Google Scholar 

  • Hanba YT, Kogami H, Terashima I (2002) The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. Plant Cell Environ 25:1021–1030

    Article  Google Scholar 

  • Hanson H (1917) Leaf-structure as related to environment. Am J Bot 4:533–560

    Article  Google Scholar 

  • Harley PC, Baldocchi DD (1995) Scaling carbon dioxide and water vapour exchange from leaf canopy in a deciduous forest. I. leaf model parametrization. Plant Cell Environ 18:1146–1156

    Article  Google Scholar 

  • Hikosaka K (2005) Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown under different temperature and light conditions: similarities and differences between temperature and light acclimation. Plant Cell Physiol 46:1283–1290

    CAS  PubMed  Google Scholar 

  • Hikosaka K, Shigeno A (2009) The role of Rubisco and cell walls in the interspecific variation in the photosynthetic capacity. Oecologia 160:443–451

    Article  PubMed  Google Scholar 

  • Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605–618

    Article  CAS  Google Scholar 

  • Hikosaka K, Terashima I (1996) Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants. Funct Ecol 10:335–343

    Article  Google Scholar 

  • Hikosaka K, Hanba YT, Hirose T, Terashima I (1998) Photosynthetic nitrogen-use efficiency in leaves of woody and herbaceous species. Funct Ecol 10:335–343

    Article  Google Scholar 

  • Hirose T, Werger MJA (1987) Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72:520–526

    Article  Google Scholar 

  • Hollinger DY (1996) Optimality and nitrogen allocation in a tree canopy. Tree Physiol 16:627–634

    Article  PubMed  Google Scholar 

  • Kirschbaum KUF, Pearcy RW (1988) Gas exchange analysis of the relative importance of stomatal and biochemical factors in photosynthetic induction in Alocasia macrorrhiza. Plant Physiol 86:782–785

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krall JP, Sheveleva EV, Pearcy RW (1995) Regulation of photosynthetic induction state in high- and low-light-grown soybean and Alocasia macrorrhiza (L.) G Don. Plant Physiol 109:307–317

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kϋlheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93

    Article  Google Scholar 

  • Le Roux X, Walcroft AS, Daudet FA, Sinoquet H, Chaves MM, Rodrigues A, Osorio L (2001) Photosynthetic light acclimation in peach leaves: importance of changes in mass: area ratio, nitrogen concentration, and leaf nitrogen partitioning. Tree Physiol 21:377–386

    Article  PubMed  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophyll a and b of leaf extracts in different solvents. Biochem Soc Trans 603:591–592

    Google Scholar 

  • Loustau D, Beahim M, Gaudillère JP, Dreyer E (1999) Photosynthetic responses to phosphorous nutrition in two-year-old maritime pine seedlings. Tree Physiol 19:707–715

    Article  PubMed  Google Scholar 

  • Meir P, Kruijt B, Broadmeadow M, Barbosa E, Kull O, Carswell F, Nobre A, Jarvis PG (2002) Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant Cell Environ 25:343–357

    Article  Google Scholar 

  • Meziane D, Shipley B (2001) Direct and indirect relationships between specific leaf area, leaf nitrogen and leaf gas exchange. Effects of irradiance and nutrient supply. Ann Bot 88:915–927

    Article  Google Scholar 

  • Montgomery R (2004) Relative importance of photosynthetic physiology and biomass allocation for tree seedling growth across a broad light gradient. Tree Physiol 24:155–167

    Article  PubMed  Google Scholar 

  • Mulkey SS, Wright SJ, Smith AP (1993) Comparative physiology and demography of three neotropical forest shrubs: alternative shade-adaptive character syndromes. Oecologia 96:526–536

    Article  Google Scholar 

  • Muller O, Hikosaka K, Hirose T (2005) Seasonal changes in light and temperature affect the balance between light harvesting and light utilization components of photosynthesis in an evergreen understory shrub. Oecologia 143:501–508

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20:845–866

    Article  Google Scholar 

  • Niinemets Ü, Bilger W, Kull O, Tenhunen JD (1998a) Acclimation to high irradiance in temperature deciduous trees in the field: changes in xanthophyll cycle pool size and in photosynthetic capacity along a canopy light gradient. Plant Cell Environ 21:1205–1218

    Article  CAS  Google Scholar 

  • Niinemets Ü, Kull O, Tenhunen JD (1998b) An analysis of light effects on foliar morphology, physiology, and light interception in temperature deciduous woody species of contrasting shade toerlance. Tree Physiol 18:681–696

    Article  PubMed  Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–512

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environ 28:916–927

    Article  Google Scholar 

  • Oguchi R, Hikosaka K, Hiura T, Hirose T (2006) Leaf anatomy and light acclimation in woody seedlings after gap formation in a cool-temperature deciduous forest. Oecologia 149:571–582

    Article  CAS  PubMed  Google Scholar 

  • Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:421–453

    CAS  Google Scholar 

  • Pearcy RW (2007) Responses of plants to heterogeneous light environments. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. CRC Press, Boca Raton, USA, pp 213–257

    Google Scholar 

  • Pearcy RW, Seemann JR (1990) Photosynthetic induction state of leaves in a soybean canopy in relation to light regulation of ribulose-1,5-bisphosphate carboxylase and stomatal conductance. Plant Physiol 94:628–633

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pearcy RW, Gross LJ, He D (1997) An improved dynamic model of photosynthesis for estimation of carbon gain in sunfleck light regimes. Plant Cell Environ 20:411–424

    Article  Google Scholar 

  • Pepin S, Livingston NJ (1997) Rates of stomatal opening in conifer seedlings in relation to air temperature and daily carbon gain. Plant Cell Environ 20:1462–1472

    Article  Google Scholar 

  • Pons TL, Pearcy RW, Seemann JR (1992) Photosynthesis in flashing light in soybean leaves in different conditions. I. Photosynthetic induction state and regulation of ribulose-1,5-bisphosphate carboxylase activity. Plant Cell Environ 15:569–576

    Article  CAS  Google Scholar 

  • Poorter L, Oberbauer SF (1993) Photosynthetic induction responses of two rainforest tree species in relation to light environment. Oecologia 96:193–199

    Article  Google Scholar 

  • Reich PB, Waters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. PANS 94:13730–13734

    Article  CAS  Google Scholar 

  • Robakowski P, Montpied P, Dreyer E (2003) Plasticity of morphological and photosynthetic traits in response to different levels of irradiance in seedlings of silver fir (Abies alba Mill). Trees 17:431–441

    Article  Google Scholar 

  • Sassenrath-Cole GF, Pearcy RW (1992) The role of ribulose-1,5-bisphoate regeneration in the induction requirement of photosynthetic CO2 exchange under transient light conditions. Plant Physiol 99:227–234

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sassenrath-Cole GF, Pearcy RW (1994) Regulation of photosynthetic induction state by the magnitude and duration of low light exposure. Plant Physiol 105:1115–1123

    CAS  PubMed Central  PubMed  Google Scholar 

  • Skillman J, Garcia M, Virgo A, Winter K (2005) Growth irradiance effects on photosynthesis and growth in two co-occurring shade-tolerant neotropical perennials of contrasting photosynthetic pathways. Am J Bot 91:1181–1819

    Google Scholar 

  • Tausz M, Warren CR, Adams MA (2005) Dynamic light use and protection from excess light in upper canopy and coppice leaves of Nothofagus cunninghamii in an old growth, cool temperature rainforest in Victoria, Australia. New Phytol 165:143–156

    Article  PubMed  Google Scholar 

  • Tazoe Y, Noguchi K, Terashima I (2006) Effects of growth light and nitrogen nutrition on the organization of the photosynthetic apparatus in leaves of a C4 plant, Amaranthus cruentus. Plant Cell Environ 29:691–700

    Article  CAS  PubMed  Google Scholar 

  • Tinoco-Ojanguren C, Pearcy RW (1993) Stomatal dynamics and its importance to carbon gain in two rainforest Piper species. II. Stomatal versus biochemical limitations during photosynthetic induction. Oecologia 94:395–402

    Article  Google Scholar 

  • Trouwborst G, Hogewoning SW, Harbinson J, van Ieperen W (2011) Photosynthetic acclimation in relation to nitrogen allocation in cucumber leaves in response to changes in irradiance. Physiol Plant 142:157–169

    Article  CAS  PubMed  Google Scholar 

  • Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111:505–514

    Article  Google Scholar 

  • Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936

    Article  Google Scholar 

  • Waters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447

    Article  Google Scholar 

  • Wyka TP, Żytkowiak R, Karolewski P, Jagodziński AM, Reich PB (2012) Responses of leaf structure and photosynthetic properties to intra-canopy light gradients: a common garden test with four broadleaf deciduous angiosperm and seven evergreen conifer tree species. Oecologia. doi:10.1007/S00442-012-2279-y

    PubMed Central  PubMed  Google Scholar 

  • Yasumura Y, Hikosaka K, Hirose T (2006) Seasonal changes in photosynthesis, nitrogen content and nitrogen partitioning in Lindera umbellate leaves grown in high or low irradiance. Tree Physiol 26:1315–1323

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura K (2010) Irradiance heterogeneity within crown affects photosynthetic capacity and nitrogen distribution of leaves in Cedrela sinensis. Plant Cell Environ 33:750–758

    CAS  PubMed  Google Scholar 

  • Zhang Q, Chen JW, Li BG, Cao KF (2009) Epiphytes and hemiepiphytes have slower photosynthetic response to lightflecks than terrestrial plants: evidence from ferns and figs. J Trop Ecol 25:465–472

    Article  Google Scholar 

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Acknowledgments

This work was funded by the National “Twelfth Five-Year” Support Project of China (Grant No. 2011BAI13B01), the Important Specific Projects of the Development and Reform Commission of Yunnan Province (Grant No. 20112513), and the National Natural Science Foundation of China (Grant No.31060094 and 81360609). We thank undergraduate students, Xiang-Zeng Xu, Shi-Shan Liu, Li-Mei Liu, Jin-Mei Wang, and Jian-Mei Zhang, for their assistance with field experiments.

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Authors and Affiliations

  1. Yunnan Research Center on Good Agricultural Practice for Dominant Chinese Medicinal Materials, Yunnan Agricultural University, Kunming, 650201, Yunnan, People’s Republic of China

    Jun-Wen Chen, Shuang-Bian Kuang, Guang-Qiang Long, Zeng-Gui Meng, Long-Gen Li, Guang-Hui Zhang & Sheng-Chao Yang

  2. Department of Crop Science, College of Agronomy and Biotechnology, Yunnan Agricultural University, Kunming, 650201, Yunnan, People’s Republic of China

    Jun-Wen Chen & Shuang-Bian Kuang

  3. Department of Plant Nutrition, College of Resource and Environment, Yunnan Agricultural University, Kunming, 650201, Yunnan, People’s Republic of China

    Guang-Qiang Long

  4. Institute of Panax Notoginseng, Wenshan University, Wenshan, 663000, Yunnan, People’s Republic of China

    Zhong-Jian Chen

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  1. Jun-Wen Chen
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  2. Shuang-Bian Kuang
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  3. Guang-Qiang Long
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  4. Zeng-Gui Meng
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Correspondence to Guang-Hui Zhang or Sheng-Chao Yang.

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Communicated by M. Garstka.

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Chen, JW., Kuang, SB., Long, GQ. et al. Steady-state and dynamic photosynthetic performance and nitrogen partitioning in the shade-demanding plant Panax notoginseng under different levels of growth irradiance. Acta Physiol Plant 36, 2409–2420 (2014). https://doi.org/10.1007/s11738-014-1614-9

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