Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Reexamining the empirical relation between plant growth and leaf photosynthesis

Eric L. Kruger A C and John C. Volin B
+ Author Affiliations
- Author Affiliations

A Department of Forest Ecology and Management, University of Wisconsin–Madison, 1630 Linden Drive, Madison, WI 53706 USA.

B Department of Biological Sciences, Florida Atlantic University, 2912 College Avenue, Davie, FL 33314 USA.

C Corresponding author. Email: elkruger@wisc.edu

D This paper originates from a presentation of ECOFIZZ 2005, North Stradbroke Island, Queensland, Australia, November 2005.

Functional Plant Biology 33(5) 421-429 https://doi.org/10.1071/FP05310
Submitted: 19 December 2005  Accepted: 3 March 2006   Published: 2 May 2006

Abstract

Technological advances during the past several decades have greatly enhanced our ability to measure leaf photosynthesis virtually anywhere and under any condition. Associated with the resulting proliferation of gas-exchange data is a lingering uncertainty regarding the importance of such measurements when it comes to explaining intrinsic causes of plant growth variation. Accordingly, in this paper we rely on a compilation of data to address the following questions: from both statistical and mechanistic standpoints, how closely does plant growth correlate with measures of leaf photosynthesis? Moreover, in this context, does the importance of leaf photosynthesis as an explanatory variable differ among growth light environments? Across a wide array of species and environments, relative growth rate (RGR) was positively correlated with daily integrals of photosynthesis expressed per unit leaf area (Aarea), leaf mass (Amass), and plant mass (Aplant). The amount of RGR variation explained by these relationships increased from 36% for the former to 93% for the latter. Notably, there was close agreement between observed RGR and that estimated from Aplant after adjustment for theoretical costs of tissue construction. Overall, based on an analysis of growth response coefficients (GRCs), gross assimilation rate (GAR), a photosynthesis-based estimate of biomass gain per unit leaf area, explained about as much growth variation as did leaf mass ratio (LMR) and specific leaf area (SLA). Further analysis of GRCs indicated that the importance of GAR in explaining growth variation increased with increasing light intensity. Clearly, when considered in combination with other key determinants, appropriate measures of leaf gas exchange effectively capture the fundamental role of leaf photosynthesis in plant growth variation.

Keywords: growth response coefficients, leaf area ratio, leaf mass ratio, net assimilation rate, relative growth rate, specific leaf area.


References


Amthor JS (1989) ‘Respiration and crop productivity.’ (Springer-Verlag: New York)

Atkin OK, Botman B, Lambers H (1996) The causes of inherently slow growth in alpine plants: an analysis based on the underlying carbon economics of alpine and lowland Poa species. Functional Ecology 10, 698–707. open url image1

Atkin OK, Schortemeyer M, McFarlane N, Evans JR (1998) Variation in the components of relative growth rate in ten Acacia species from contrasting environments. Plant, Cell & Environment 21, 1007–1017.
Crossref | GoogleScholarGoogle Scholar | open url image1

Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Functional Plant Biology 32, 87–105.
Crossref | GoogleScholarGoogle Scholar | open url image1

Blackman VH (1919) The compound interest law and plant growth. Annals of Botany 33, 353–360. open url image1

Bunce JA (1995) Effects of elevated carbon dioxide concentration in the dark on the growth of soybean seedlings. Annals of Botany 75, 365–368.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chapin FS (1989) The cost of tundra plant structures: evaluation of concepts and currencies. American Naturalist 133, 1–19.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cornelissen JHC, Diez PC, Hunt R (1996) Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types. Journal of Ecology 84, 755–765. open url image1

Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant, Cell & Environment 21, 427–435.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cramer GR, Nowack RS (1992) Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt-stressed barley. Physiologia Plantarum 84, 600–605.
Crossref | GoogleScholarGoogle Scholar | open url image1

De Jong TM (1978) Comparative gas exchange and growth responses of C3 and C4 beach species grown at different salinities. Oecologia 36, 59–68.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dijkstra P (1989) Cause and effect of differences in specific leaf area. In ‘Causes and consequences of variation in growth rate and productivity of higher plants’. (Eds H Lambers, ML Cambridge, H Konings, TL Pons) pp. 101–123. (SPB Academic Publishing: The Hague)

Dijkstra P , Lambers H (1986) Photosynthesis and respiration of two inbred lines of Plantago major L. differing in relative growth rate. In ‘Biological control of photosynthesis’. (Eds R Marcelle, H Clijsters, M Van Poucke) pp. 251–255. (Martinus Nijhoff Publishers: Dordrecht)

Donaldson JR, Kruger EL, Lindroth RL (2006) Stress-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytologist 169, 561–570.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Evans GC (1972) ‘The quantitative analysis of plant growth.’ (Blackwell Scientific Publications: Oxford)

Evans LT (1975) ‘Crop physiology: some case histories.’ (Cambridge University Press: Cambridge)

Fetene M, Feleke Y (2001) Growth and photosynthesis of seedlings of four tree species from a dry tropical afromontane forest. Journal of Tropical Ecology 17, 269–283.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gifford RM, Evans LT (1981) Photosynthesis, carbon partitioning and yield. Annual Review of Plant Physiology 32, 485–509.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hanson PJ, McRoberts E, Isebrands JG, Dixon RK (1987) An optimal sampling strategy for determining CO2 exchange rate as a function of photosynthetic photon flux density. Photosynthetica 21, 98–101. open url image1

Harrington RA, Fownes JH, Cassidy TM (2004) Japanese barberry (Berberis thunbergii) in forest understory: leaf and whole plant responses to nitrogen availability. American Midland Naturalist 151, 206–216. open url image1

den Hertog J, Stulen I, Posthumus F, Poorter H (1998) Interactive effects of growth-limiting N supply and elevated atmospheric CO2 concentration on growth and carbon balance of Plantago major. Physiologia Plantarum 103, 451–460.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huante P, Rincon E (1998) Responses to light changes in tropical deciduous woody seedlings with contrasting growth rates. Oecologia 113, 53–66.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huante P, Rincon E, Acosta I (1995) Nutrient availability and growth rate of 34 woody species from a tropical deciduous forest in Mexico. Functional Ecology 9, 849–858. open url image1

Jansen CM , Pot S , Lambers H (1986) The influence of CO2 enrichment of the atmosphere and NaCl on growth and metabolism of Urtica dioica L. In ‘Biological control of photosynthesis’. (Eds R Marcelle, H Clijsters, M Van Poucke) pp. 143–146. (Martinus Nijhoff Publishers: Dordrecht)

Kaelke CM, Kruger EL, Reich PB (2001) Trade-offs in seedling survival, growth, and physiology among hardwood species of contrasting successional status along a light-availability gradient. Canadian Journal of Forest Research 31, 1602–1616.
Crossref | GoogleScholarGoogle Scholar | open url image1

Konings H (1989) Physiological and morphological differences between plants with a high NAR or a high LAR as related to environmental conditions. In ‘Causes and consequences of variation in growth rate and productivity of higher plants’. (Eds H Lambers, ML Cambridge, H Konings, TL Pons) pp. 101–123. (SPB Academic Publishing: The Hague)

Konings H, Koot E, Tijman-de Wolf A (1989) Growth characteristics, nutrient allocation and photosynthesis of Carex species from floating fens. Oecologia 80, 111–121.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research 23, 188–261. open url image1

Lawlor DW (1995) Photosynthesis, productivity and environment. Journal of Experimental Botany 46, 1449–1461. open url image1

Lerdau M, Guenther A, Monson R (1997) Plant production and emission of volatile organic compounds. Bioscience 47, 373–383.
Crossref |
open url image1

Loveys BR, Scheurwater I, Pons TL, Fitter AH, Atkin OK (2002) Growth temperature influences the underlying components of relative growth rate: an investigation using inherently fast- and slow-growing plant species. Plant, Cell & Environment 25, 975–987.
Crossref | GoogleScholarGoogle Scholar | open url image1

Norby RJ, O’Neill EG (1991) Leaf area compensation and nutrient interactions in CO2-enriched seedlings of yellow-poplar (Liriodendron tulipifera L.). New Phytologist 117, 515–528. open url image1

Peng S, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiology 101, 1063–1071.
PubMed |
open url image1

Poorter H (1994) Construction costs and payback time of biomass: a whole-plant perspective. In ‘A whole-plant perspective on carbon–nitrogen interactions’. (Eds J Roy, E Garnier) pp. 111–127. (SPB Academic Publishing: The Hague)

Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553–559.
Crossref | GoogleScholarGoogle Scholar | open url image1

Poorter H, Bergkotte M (1992) Chemical composition of 24 wild species differing in relative growth rate. Plant, Cell & Environment 15, 221–229. open url image1

Poorter H, Pothmann P (1992) Growth and carbon economy of a fast-growing and a slow-growing grass species as dependent on ontogeny. New Phytologist 120, 159–166. open url image1

Poorter H , van der Werf A (1998) Is inherent variation in RGR determined by LAR at low irradiance and by NAR at high irradiance? A review of herbaceous species. In ‘Inherent variation in plant growth: physiological mechanisms and ecological consequences’. (Eds H Lambers, H Poorter, MMI Van Vuuren) pp. 309–336. (Backhuys: Leiden)

Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiology 94, 621–627. open url image1

Poorter H, van Rijn CPE, Vanhala TK, Verhoeven KJF, de Jong YEM, Stam P, Lambers H (2005) A genetic analysis of relative growth rate and underlying components in Hordeum spontaneum. Oecologia 142, 360–377.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reich PB, Uhl C, Walters MB, Ellsworth DS (1991) Leaf lifespan as a determinant of leaf structure and function among 23 Amazonian tree species. Oecologia 86, 16–24.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rice SA, Bazzaz FA (1989) Quantification of plasticity of plant traits in response to light intensity: comparing phenotypes at a common weight. Oecologia 78, 502–507.
Crossref | GoogleScholarGoogle Scholar | open url image1

van Rijn CPE, Heersche I, van Berkel YEM, Nevo E, Lambers H, Poorter H (2000) Growth characteristics in Hordeum spontaneum populations from different habitats. New Phytologist 146, 471–481.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryle JA, Powell CE, Tewson V (1992) Effect of elevated CO2 on the photosynthesis, respiration and growth of perennial ryegrass. Journal of Experimental Botany 43, 811–818. open url image1

Sharkey TD, Yeh S (2001) Isoprene emission from plants. Annual Review of Plant Physiology and Plant Molecular Biology 52, 407–436.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sharkey TD, Loreto F, Delwiche CF (1991) High carbon dioxide and sun / shade effects on isoprene emission from oak and aspen tree leaves. Plant, Cell & Environment 14, 333–338. open url image1

Sharkey TD , Laporte MM , Kruger EL (2000) Will increased photosynthetic efficiency lead to increased yield in rice? In ‘The quest to reduce hunger: redesigning rice photosynthesis’. (Ed. J Sheehy) pp. 73–86. (IRRI: Los Baños and Elsevier Science: Amsterdam)

Shipley B (2002) Trade-offs between net assimilation rate and specific leaf area in determining relative growth rate: relationship with daily irradiance. Functional Ecology 16, 682–689.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tjoelker MG, Oleksyn J, Reich PB (1998) Seedlings of five boreal tree species differ in acclimation of net photosynthesis to elevated CO2 and temperature. Tree Physiology 18, 715–726.
PubMed |
open url image1

Turner AD, Wien HC (1994) Photosynthesis, dark respiration and bud sugar concentrations in pepper cultivars differing in susceptibility to stress-induced bud abscission. Annals of Botany 73, 623–628.
Crossref | GoogleScholarGoogle Scholar | open url image1

van Veen JA, Liljeroth E, Lekkerkerk LJA, Van De Geijn SC (1991) Carbon fluxes in plant–soil systems at elevated atmospheric CO2 levels. Ecological Applications 1, 175–181.
Crossref |
open url image1

Veneklaas EJ , Poorter H (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: Leiden)

Veneklaas EJ, Santos Silva MPRM, den Ouden F (2002) Determinants of growth rate in Ficus benjamina L. compared to related faster-growing woody and herbaceous species. Scientia Horticulturae 93, 75–84.
Crossref | GoogleScholarGoogle Scholar | open url image1

Volin JC, Kruger EL, Lindroth RL (2002) Responses of deciduous broadleaf trees to defoliation in a CO2 enriched atmosphere. Tree Physiology 22, 435–448.
PubMed |
open url image1

Walters MB, Kruger EL, Reich PB (1993) Relative growth rate in relation to physiological and morphological traits for northern hardwood tree seedlings: species, light environment and ontogenetic considerations. Oecologia 96, 219–231.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warren CR, Adams MA (2005) What determines interspecific variation in relative growth rate of Eucalyptus seedlings? Oecologia 144, 373–381.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wright IJ, Westoby M (1999) Differences in seedling growth behavior among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients. Journal of Ecology 87, 85–97.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zelitch I (1982) The close relationship between net photosynthesis and crop yield. Bioscience 32, 796–802.
Crossref |
open url image1