Relative contributions of light interception and radiation use efficiency to the reduction of maize productivity under cold temperatures
Gaëtan Louarn A E , Karine Chenu A D , Christian Fournier B C , Bruno Andrieu B C and Catherine Giauffret AA INRA, UMR 1281 SADV, F-80203 Estrées-Mons, France.
B INRA, UMR 1091 EGC, F-78850 Thiverval-Grignon, France.
C AgroParisTech, UMR 1091 EGC, F-78850 Thiverval-Grignon, France.
D Present address: APSRU, Department of Primary Industries and Fisheries, PO Box 102, Toowoomba, Qld 4350, Australia.
E Corresponding author. Email: gaetan.louarn@mons.inra.fr
This paper originates from a presentation at the 5th International Workshop on Functional–Structural Plant Models, Napier, New Zealand, November 2007.
Functional Plant Biology 35(10) 885-899 https://doi.org/10.1071/FP08061
Submitted: 8 March 2008 Accepted: 28 July 2008 Published: 11 November 2008
Abstract
Maize (Zea mays L.) is a chill-susceptible crop cultivated in northern latitude environments. The detrimental effects of cold on growth and photosynthetic activity have long been established. However, a general overview of how important these processes are with respect to the reduction of productivity reported in the field is still lacking. In this study, a model-assisted approach was used to dissect variations in productivity under suboptimal temperatures and quantify the relative contributions of light interception (PARc) and radiation use efficiency (RUE) from emergence to flowering. A combination of architectural and light transfer models was used to calculate light interception in three field experiments with two cold-tolerant lines and at two sowing dates. Model assessment confirmed that the approach was suitable to infer light interception. Biomass production was strongly affected by early sowings. RUE was identified as the main cause of biomass reduction during cold events. Furthermore, PARc explained most of the variability observed at flowering, its relative contributions being more or less important according to the climate experienced. Cold temperatures resulted in lower PARc, mainly because final leaf length and width were significantly reduced for all leaves emerging after the first cold occurrence. These results confirm that virtual plants can be useful as fine phenotyping tools. A scheme of action of cold on leaf expansion, light interception and radiation use efficiency is discussed with a view towards helping breeders define relevant selection criteria.
Additional keywords: architecture, chilling stress, elite inbreds, light transfer model, structural model, Zea mays.
Acknowledgements
This study was supported by the Conseil Régional de Picardie (www.cr-picardie.fr) and INRA (www.inra.fr), France. We are grateful to M. Chelle for making the light transfer model available. We would also like to thank I Dourlen, J-F Hû and D. Rabier for their help with the experiment, and J. Hillier for the improvement of the manuscript.
Aguilera C,
Stirling CM, Long SP
(1999) Genotypic variation within Zea mays for susceptibility to and rate of recovery from chill-induced photoinhibition of photosynthesis. Physiologia Plantarum 106, 429–436.
| Crossref | GoogleScholarGoogle Scholar |
Andrieu B,
Hillier J, Birch C
(2006) Onset of sheath extension and duration of lamina extension are major determinants of the response of maize lamina length to plant density. Annals of Botany 98, 1005–1016.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ben Haj Salah H, Tardieu F
(1995) Temperature affects expansion rate of maize leaves without change in spatial distribution of cell length. Analysis of the coordination between cell division and cell expansion. Plant Physiology 109, 861–870.
| PubMed |
Blondon F,
Clabault G, Rainguez M
(1980) Action d’une température fraîche (10°C) appliquée au stade jeune sur la croissance et l’activité photosynthétique de deux variétés précoces de Maïs. Annales d’Amélioration des Plantes 30, 399–410.
Bonhomme R
(2000) Beware of comparing RUE values calculated from PAR vs. solar radiation or absorbed vs. intercepted radiation. Field Crops Research 68, 247–252.
| Crossref | GoogleScholarGoogle Scholar |
Bonhomme R, Varlet-Grancher C
(1978) Estimation of the gramineous crop geometry by plant profiles including leaf width variations. Photosynthetica 12, 193–196.
Campbell CS,
Heilman JL,
McInnes KJ,
Wilson LT,
Medley JC,
Wu G, Cobos DR
(2001) Seasonal variation in radiation use efficiency of irrigated rice. Agricultural and Forest Meteorology 110, 45–54.
| Crossref | GoogleScholarGoogle Scholar |
Casella E, Sinoquet H
(2003) A method for describing the canopy architecture of coppice poplar with allometric relationships. Tree Physiology 23, 1153–1170.
| PubMed |
Chelle C, Andrieu B
(1998) The nested radiosity model for the distribution of light within plant canopies. Ecological Modelling 111, 75–91.
| Crossref | GoogleScholarGoogle Scholar |
Chenu K,
Franck N,
Dauzat J,
Barczi JF,
Rey H, Lecoeur J
(2005) Integrated responses of rosette organogenesis, morphogenesis and architecture to reduced incident light in Arabidopsis thaliana results in higher efficiency of light interception. Functional Plant Biology 32, 1123–1134.
| Crossref | GoogleScholarGoogle Scholar |
Chenu K,
Franck N, Lecoeur J
(2007) Simulations of virtual plants reveal a role for SERRATE in the response of leaf development to light in Arabidopsis thaliana. New Phytologist 175, 472–481.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chenu K,
Chapman SC,
Hammer GL,
McLean G, Tardieu F
(2008a) Short term responses of leaf growth rate to water deficit scale up to whole-plant and crop levels. An integrated modelling approach in maize. Plant, Cell & Environment 31, 378–391.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chenu K,
Rey H,
Dauzat J,
Lydie G, Lecœur J
(2008b) Estimation of light interception in research environments: a joint approach using directional light sensors and 3D virtual plants applied to sunflower (Helianthus annuus) and Arabidopsis thaliana in natural and artificial conditions. Functional Plant Biology 35, 850–866.
Dolstra O,
Haalstra SR,
Van der Putten PEL, Schapendonk AHCM
(1994) Genetic variation for resistance to low temperature photoinhibition of photosynthesis in maize. Euphytica 80, 85–93.
| Crossref | GoogleScholarGoogle Scholar |
Eagles HA, Hardacre AK
(1979) Genetic variation in maize (Zea mays L.) for germination and emergence at 10°C. Euphytica 28, 287–295.
| Crossref | GoogleScholarGoogle Scholar |
Evers JB,
Vos J,
Fournier C,
Andrieu B,
Chelle M, Struik PC
(2007) An architectural model of spring wheat: evaluation of the effects of population density and shading on model parameterization and performance. Ecological Modelling 200, 308–320.
| Crossref | GoogleScholarGoogle Scholar |
Fournier C, Andrieu B
(1998) A 3-D architectural and process-based model of maize development. Annals of Botany 81, 233–250.
| Crossref | GoogleScholarGoogle Scholar |
Fournier C,
Durand JL,
Ljutovac S,
Schäufele R,
Gastal F, Andrieu B
(2005) A functional–structural model of elongation of the grass leaf and its relationships with the phyllochron. New Phytologist 166, 881–894.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fracheboud Y,
Jompuk C,
Ribaut J,
Stamp P, Leipner J
(2004) Genetic analysis of cold-tolerance of photosynthesis in maize. Plant Molecular Biology 56, 241–253.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fryer MJ,
Oxborough K,
Martin B,
Ort DR, Baker NR
(1995) Factors associated with depression of photosynthetic quantum efficiency in maize at low growth temperature. Plant Physiology 108, 761–767.
| PubMed |
Gallo KP, Daughtry CST
(1986) Techniques for measuring intercepted and absorbed photosynthetically active radiation in corn canopies. Agronomy Journal 78, 752–756.
Giauffret C,
Bonhomme R, Derieux M
(1995) Genotypic differences for temperature response of leaf appearance rate and leaf elongation rate in field-grown maize. Agronomie 15, 123–137.
| Crossref | GoogleScholarGoogle Scholar |
Greaves JA
(1996) Improving suboptimal temperature tolerance in maize – the search for variation. Journal of Experimental Botany 47, 307–323.
| Crossref | GoogleScholarGoogle Scholar |
Greer DH, Hardacre AK
(1989) Photoinhibition of photosynthesis and its recovery in two maize hybrids varying in low temperature tolerance. Australian Journal of Plant Physiology 16, 189–198.
Haldimann P
(1998) Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays L. genotypes differing in chilling sensitivity. Plant, Cell & Environment 21, 200–208.
| Crossref | GoogleScholarGoogle Scholar |
Hall AJ,
Connor DJ, Sadras VO
(1995) Radiation use efficiency of sunflower crop: effects of specific leaf nitrogen and ontogeny. Field Crops Research 41, 65–77.
| Crossref | GoogleScholarGoogle Scholar |
Heath MC, Hebblethwaite PD
(1987) Seasonal radiation interception, dry matter production and yield determination for a semi-leafless pea (Pisum sativum) breeding selection under contrasting field conditions. Annals of Applied Biology 110, 413–420.
| Crossref | GoogleScholarGoogle Scholar |
Hutchinson BA,
Matt DR, McMillen RT
(1980) Effect of sky brightness distribution upon penetration of diffuse radiation through canopy gaps in a deciduous forest. Agricultural and Forest Meteorology 22, 137–147.
Janda T,
Szalai G,
Ducruet JM, Páldi E
(1998) Changes in photosynthesis in inbred maize lines with different degrees of chilling tolerance grown at optimum and suboptimum temperatures. Photosynthetica 35, 205–212.
| Crossref | GoogleScholarGoogle Scholar |
Jompuk C,
Fracheboud Y,
Stamp P, Leipner J
(2005) Mapping of quantitative trait loci associated with chilling tolerance in maize (Zea mays L.) seedlings grown under field conditions. Journal of Experimental Botany 56, 1153–1163.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lauer JG,
Carter PR,
Wood TM,
Diezel G,
Wiersma DW,
Rand RE, Mlynarek MJ
(1999) Corn hybrid response to planting date in the northern corn belt. Agronomy Journal 91, 834–839.
Lecoeur J, Ney B
(2003) Change with time in potential radiation use efficiency in field pea. European Journal of Agronomy 19, 91–105.
| Crossref | GoogleScholarGoogle Scholar |
Lee EA,
Staebler MA, Tollenaar M
(2002) Genetic variation in physiological discriminators for cold tolerance – early autotrophic phase of maize development. Crop Science 42, 1919–1929.
Leipner J,
Jompuk C,
Camp KH,
Stamp P, Fracheboud Y
(2008) QTL studies reveal little relevance of chilling-related seedling traits for yield in maize. Theoretical and Applied Genetics 116, 555–562.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Letort V,
Mahe P,
Cournede P-H,
De Reffye P, Courtois B
(2008) Quantitative genetics and functional–structural plant growth models: simulation of quantitative trait loci detection for model parameters and application to potential yield optimization. Annals of Botany 101, 1243–1254.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lindquist JL,
Arkebauer TJ,
Walters DT,
Cassman KG, Dobermann A
(2005) Maize radiation use efficiency under optimal growth conditions. Agronomy Journal 97, 72–78.
Long SP
(1983) C4 photosynthesis at low temperatures. Plant, Cell & Environment 6, 345–363.
Long SP,
East TM, Baker NR
(1983) Chilling damage to photosynthesis in young Zea mays. I. Effects of light and temperature variation on photosynthetic CO2 assimilation. Journal of Experimental Botany 34, 177–188.
| Crossref | GoogleScholarGoogle Scholar |
Louarn G,
Lecoeur J, Lebon E
(2008a) A three-dimensional statistical reconstruction model of grapevine (Vitis vinifera) simulating canopy structure variability within and between cultivar/training system pairs. Annals of Botany 101, 1167–1184.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Louarn G,
Dauzat J,
Lecoeur J, Lebon E
(2008b) Influence of trellis system and shoot positioning on light interception and distribution in two grapevine cultivars with different architectures – an original approach based on 3-D canopy modelling. Australian Journal of Grape and Wine Research in press ,
Luquet D,
Song YH,
Elbert S,
This D,
Clément-Vidal A,
Périn C,
Fabre D, Dingkuhn M
(2007) Model-assisted physiological analysis of Phyllo, a rice architectural mutant. Functional Plant Biology 34, 11–23.
| Crossref | GoogleScholarGoogle Scholar |
Maddonni GA,
Otegui ME, Cirilo AG
(2001) Plant population density, row spacing and hybrid effects on maize canopy architecture and light attenuation. Field Crops Research 71, 183–193.
| Crossref | GoogleScholarGoogle Scholar |
Massacci A,
Iannelli MA,
Pietrini F, Loreto F
(1995) The effect of growth at low temperature on photosynthetic characteristics and mecanisms of photoprotection of maize leaves. Journal of Experimental Botany 34, 177–188.
Massad RS,
Tuzet A, Bethenod O
(2007) The effect of temperature on C4-type leaf photosynthesis parameters. Plant, Cell & Environment 30, 1191–1204.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Meiri A,
Silk WK, Lauchli A
(1992) Growth and deposition of inorganic nutrient elements in developing leaves of Zea mays L. Plant Physiology 98, 972–978.
Miedema P
(1982) The effect of low temperature on Zea mays. Advances in Agronomy 35, 93–128.
| Crossref | GoogleScholarGoogle Scholar |
Monteith JL
(1977) Climate and efficiency of crop production in Britain. Philosophical Transactions of the Royal Society of London 281, 277–294.
| Crossref | GoogleScholarGoogle Scholar |
Nie G-Y,
Robertson EJ,
Fryer MJ,
Leech RM, Baker NR
(1995) Response of the photosynthetic apparatus in maize leaves grown at low temperature on transfer to normal temperature. Plant, Cell & Environment 18, 1–12.
| Crossref | GoogleScholarGoogle Scholar |
Padilla JM, Otegui ME
(2005) Co-ordination between leaf initiation and leaf appearance in field-grown maize (Zea mays): genotypic differences in response of rates to temperature. Annals of Botany 96, 997–1007.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pearce RS
(1999) Molecular analysis of acclimation to cold. Plant Growth Regulation 29, 47–76.
| Crossref | GoogleScholarGoogle Scholar |
Pearcy RW, Yang W
(1996) A three-dimensional crown architecture model for assessment of light capture and carbon gain by understory plants. Oecologia 108, 1–12.
| Crossref | GoogleScholarGoogle Scholar |
Prévot L,
Aries F, Monestiez P
(1991) Modélisation de la structure géométrique du maïs. Agronomie 11, 491–503.
| Crossref | GoogleScholarGoogle Scholar |
Rey H,
Dauzat J,
Chenu K,
Barczi JF,
Dosio JAA, Lecoeur J
(2008) Using a 3-D virtual sunflower to simulate light capture at organ, plant and plot levels: contribution of organ interception, impact of heliotropism and analysis of genotypic differences. Annals of Botany in press ,
Reynolds MP,
van Ginkel M, Ribaut J-M
(2000) Avenues for genetic modification of radiation use efficiency in wheat. Journal of Experimental Botany 51, 459–473.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Richner W,
Soldati A, Stamp P
(1995) Shoot-root relations in field-grown maize seedlings. Agronomy Journal 88, 51–61.
Rochette P,
Desjardins RL,
Pattey E, Lessard R
(1996) Instantaneous measurements of radiation and water use efficiency of a maize crop. Agronomy Journal 88, 627–635.
Ruget F,
Bonhomme R, Chartier M
(1996) Estimation simple de la surface foliaire de plantes de maïs en croissance. Agronomie 16, 553–562.
| Crossref | GoogleScholarGoogle Scholar |
Rymen B,
Fiorani F,
Kartal F,
Vanderpoele K,
Inzé D, Beemster G
(2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiology 143, 1429–1438.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sinclair TR, Horie T
(1989) Leaf nitrogen, photosynthesis and crop radiation use efficiency: a review. Crop Science 29, 90–98.
Sinclair TR, Muchow RC
(1999) Radiation use efficiency. Advances in Agronomy 65, 215–265.
| Crossref | GoogleScholarGoogle Scholar |
Smillie RM,
Hetherington SE,
He J, Nott R
(1988) Photoinhibition at chilling temperatures. Australian Journal of Plant Physiology 15, 207–222.
Sowiński P,
Rudzińska-Langwald A, Kobus P
(2003) Changes in plasmodesmata frequency in vascular bundles of the leaf of Zea mays L. seedlings induced by growth at suboptimal temperatures in relation to photosynthesis and assimilate export. Environmental and Experimental Botany 50, 183–196.
| Crossref | GoogleScholarGoogle Scholar |
Sowiński P,
Ridzińska-Langwald A,
Adamczyk J,
Kubica I, Fronk J
(2005) Recovery of maize seedling growth, development and photosynthetic efficiency after initial growth at low temperature. Journal of Plant Physiology 162, 67–80.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Spitters CJT,
Toussaint HAJM, Goudriaan J
(1986) Separating the diffuse and direct component of global radiation and its implications for modeling canopy photosynthesis. 1. Components of incoming radiation. Agricultural and Forest Meteorology 38, 217–229.
| Crossref | GoogleScholarGoogle Scholar |
Verheul MJ,
van Hasselt PR, Stamp P
(1995) Comparison of maize inbred lines differing in low temperature tolerance: effect of acclimation at suboptimal temperature on chloroplast functioning. Annals of Botany 76, 7–14.
| Crossref | GoogleScholarGoogle Scholar |
Verheul MJ,
Picatto C, Stamp P
(1996) Growth and development of maize (Zea mays L.) seedlings under chilling conditions in the field. European Journal of Agronomy 5, 31–41.
| Crossref | GoogleScholarGoogle Scholar |
Westgate ME,
Forcella F,
Reicosky DC, Somsen J
(1997) Rapid canopy closure for maize production in the northern US corn belt: radiation-use efficiency and grain yield. Field Crops Research 49, 249–258.
| Crossref | GoogleScholarGoogle Scholar |
Yan W, Hunt LA
(1999) An equation for modeling the temperature response of plants using only the cardinal temperatures. Annals of Botany 84, 607–614.
| Crossref | GoogleScholarGoogle Scholar |
Ying J,
Lee EA, Tollenaar M
(2000) Response of maize leaf photosynthesis to low temperature during the grain-filling period. Field Crops Research 68, 87–96.
| Crossref | GoogleScholarGoogle Scholar |
