Heterogeneity of photosynthesis within leaves is associated with alteration of leaf structural features and leaf N content per leaf area in rice
Dongliang Xiong A , Tingting Yu A , Xi Liu A , Yong Li A , Shaobing Peng A and Jianliang Huang A B CA National Key Laboratory of Crop Genetic Improvement, MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China.
B Hubei Collaborative Innovation Center for Grain Industry, Yangtze University, Jingzhou, Hubei 434023, China.
C Corresponding author. Email: jhuang@mail.hzau.edu.cn
Functional Plant Biology 42(7) 687-696 https://doi.org/10.1071/FP15057
Submitted: 20 December 2014 Accepted: 11 April 2015 Published: 20 May 2015
Abstract
Increasing leaf photosynthesis rate (A) is considered an important strategy to increase C3 crop yields. Leaf A is usually represented by point measurements, but A varies within each leaf, especially within large leaves. However, little is known about the effect of heterogeneity of A within leaves on rice performance. Here we investigated the changes in gas-exchange parameters and leaf structural and chemical features along leaf blades in two rice cultivars. Stomatal and mesophyll conductance as well as leaf nitrogen (N), Rubisco and chlorophyll contents increased from base to apex; consequently, A increased along leaves in both cultivars. The variation in A, leaf N content and Rubisco content within leaves was similar to the variations among cultivars, and the extent of A heterogeneity within leaves varied between cultivars, leading to different efficiencies of biomass accumulation. Furthermore, variation of A within leaves was closely associated with leaf structural and chemical features. Our findings emphasise that functional changes along leaf blades are associated with structural and chemical trait variation and that variation of A within leaves should be considered to achieve progress in future breeding programs.
Additional keywords: biomass, CO2 diffusion, leaf structure, leaf N content per leaf area.
References
Aliniaeifard S, van Meeteren U (2014) Natural variation in stomatal response to closing stimuli among Arabidopsis thaliana accessions after exposure to low VPD as a tool to recognise the mechanism of disturbed stomatal functioning. Journal of Experimental Botany 65, 6529–6542.| Natural variation in stomatal response to closing stimuli among Arabidopsis thaliana accessions after exposure to low VPD as a tool to recognise the mechanism of disturbed stomatal functioning.Crossref | GoogleScholarGoogle Scholar | 25205580PubMed |
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
| Leaf maximum photosynthetic rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=29d8261142c5c49e1d2bf94275d52766CAS | 17556506PubMed |
Brooks A, Farquhar G (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397–406.
| Effect of temperature on the CO2/O2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltlyrsLc%3D&md5=87ef81a2b975d3d5159f4be09ccd969bCAS | 24241146PubMed |
Creese C, Oberbauer S, Rundel P, Sack L (2014) Are fern stomatal responses to different stimuli coordinated? Testing responses to light, vapor pressure deficit, and CO2 for diverse species grown under contrasting irradiances. New Phytologist 204, 92–104.
| Are fern stomatal responses to different stimuli coordinated? Testing responses to light, vapor pressure deficit, and CO2 for diverse species grown under contrasting irradiances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVGhur3N&md5=4a4ac667cf120875cdcdb9b55f2d1bb3CAS | 25077933PubMed |
Dow GJ, Berry JA, Bergmann DC (2014) The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. New Phytologist 201, 1205–1217.
| The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVegsr4%3D&md5=db21353401f0f072ef0c31f8b43f5a20CAS | 24206523PubMed |
Drake PL, Froend RH, Franks PJ (2013) Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance. Journal of Experimental Botany 64, 495–505.
| Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntVGltg%3D%3D&md5=4dc2def604106d83bddf049850156b23CAS | 23264516PubMed |
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
| Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |
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 |
Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell & Environment 31, 602–621.
| Mesophyll conductance to CO2: current knowledge and future prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvFehtbc%3D&md5=13525cdbd81f49d1a74aa7c618d7379cCAS |
Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, Peguero-Pina JJ, Pou A, Ribas-Carbó M, Tomás M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis. Plant Science 193–194, 70–84.
| Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 22794920PubMed |
Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106, 10343–10347.
| Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXot1Giurg%3D&md5=670135a6e48c6655eb94cd3eab4a952aCAS | 19506250PubMed |
Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant, Cell & Environment 32, 1737–1748.
| Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |
Giuliani R, Koteyeva N, Voznesenskaya E, Evans MA, Cousins AB, Edwards GE (2013) Coordination of leaf photosynthesis, transpiration, and structural traits in rice and wild relatives (Genus Oryza). Plant Physiology 162, 1632–1651.
| Coordination of leaf photosynthesis, transpiration, and structural traits in rice and wild relatives (Genus Oryza).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFCmtLbE&md5=614857bc32a47c9ea2a7eaac62df1f4aCAS | 23669746PubMed |
Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiology 98, 1429–1436.
| Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XisFagu7o%3D&md5=ea18929283f91c7ea3f9421be0a0a193CAS | 16668811PubMed |
Hikosaka K, Terashima I (1996) Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants. Functional Ecology 10, 335–343.
| Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants.Crossref | GoogleScholarGoogle Scholar |
Hirasawa T, Ozawa S, Taylaran RD, Ookawa T (2010) Varietal differences in photosynthetic rates in rice plants, with special reference to the nitrogen content of leaves. Plant Production Science 13, 53–57.
| Varietal differences in photosynthetic rates in rice plants, with special reference to the nitrogen content of leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVWhtLk%3D&md5=ff5b2f4b22b18f8d0b09d86e0096cbe2CAS |
Kamakura M, Kosugi Y, Takanashi S, Matsumoto K, Okumura M, Philip E (2011) Patchy stomatal behavior during midday depression of leaf CO2 exchange in tropical trees. Tree Physiology 31, 160–168.
| Patchy stomatal behavior during midday depression of leaf CO2 exchange in tropical trees.Crossref | GoogleScholarGoogle Scholar | 21383025PubMed |
Khush GS (2001) Green revolution: the way forward. Nature Reviews. Genetics 2, 815–822.
| Green revolution: the way forward.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmt1Wgu7w%3D&md5=8ebe4e5b8c4189e5992ed86a76d73a73CAS | 11584298PubMed |
Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiology 164, 1556–1570.
| Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsVyqu7s%3D&md5=ace5a7c0170498f835e7caa0f0553954CAS | 24578506PubMed |
Li Y, Gao Y, Xu X, Shen Q, Guo S (2009) Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration. Journal of Experimental Botany 60, 2351–2360.
| Light-saturated photosynthetic rate in high-nitrogen rice (Oryza sativa L.) leaves is related to chloroplastic CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlyitbg%3D&md5=ac569298a2586cdde706df74fddc73c8CAS | 19395387PubMed |
Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany 54, 2393–2401.
| Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVert7s%3D&md5=10d936105a28a035f62e628cf442af4fCAS | 14512377PubMed |
Long SP, Zhu X-G, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant, Cell & Environment 29, 315–330.
| Can improvement in photosynthesis increase crop yields?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyltrw%3D&md5=6afa5628a843228382a604400ba781e7CAS |
Makino A, Mae T, Ohira K (1985) Enzymic properties of Ribulose-1,5-bisphosphate carboxylase/oxygenase purified from rice leaves. Plant Physiology 79, 57–61.
| Enzymic properties of Ribulose-1,5-bisphosphate carboxylase/oxygenase purified from rice leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvFahsb4%3D&md5=8e4f3a0cf21d721acf8c225df91ba886CAS | 16664401PubMed |
Meinzer FC, Saliendra NZ (1997) Spatial patterns of carbon isotope discrimination and allocation of photosynthetic activity in sugarcane leaves. Functional Plant Biology 24, 769–775.
Mitchell PL, Sheehy JE (2006) Supercharging rice photosynthesis to increase yield. New Phytologist 171, 688–693.
| Supercharging rice photosynthesis to increase yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVSku77L&md5=abafda98394e14a1713d8182c4ea0498CAS | 16918541PubMed |
Mott KA (1995) Effects of patchy stomatal closure on gas exchange measurements following abscisic acid treatment. Plant, Cell & Environment 18, 1291–1300.
| Effects of patchy stomatal closure on gas exchange measurements following abscisic acid treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xot1Wh&md5=e40d3f7f5929b46b6dad6fc544565130CAS |
Mott KA, Peak D (2007) Stomatal patchiness and task-performing networks. Annals of Botany 99, 219–226.
| Stomatal patchiness and task-performing networks.Crossref | GoogleScholarGoogle Scholar | 17085471PubMed |
Muir CD, Hangarter RP, Moyle LC, Davis PA (2014) Morphological and anatomical determinants of mesophyll conductance in wild relatives of tomato (Solanum sect. Lycopersicon, sect. Lycopersicoides; Solanaceae). Plant, Cell & Environment 37, 1415–1426.
| Morphological and anatomical determinants of mesophyll conductance in wild relatives of tomato (Solanum sect. Lycopersicon, sect. Lycopersicoides; Solanaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntlWns7w%3D&md5=309f73b204a80216a8c197ae6deffdb6CAS |
Ocheltree TW, Nippert JB, Prasad PVV (2012) Changes in stomatal conductance along grass blades reflect changes in leaf structure. Plant, Cell & Environment 35, 1040–1049.
| Changes in stomatal conductance along grass blades reflect changes in leaf structure.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zosVGhtQ%3D%3D&md5=04713ec35a19ae95394cb947d9b25013CAS |
Osada N, Yasumura Y, Ishida A (2014) Leaf nitrogen distribution in relation to crown architecture in the tall canopy species, Fagus crenata. Oecologia 175, 1093–1106.
| Leaf nitrogen distribution in relation to crown architecture in the tall canopy species, Fagus crenata.Crossref | GoogleScholarGoogle Scholar | 24844645PubMed |
Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87, 483–491.
| Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar | 16637372PubMed |
Sack L, Holbrook NM (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361–381.
| Leaf hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhtrs%3D&md5=49498cc5040720b733d957859a88abfcCAS | 16669766PubMed |
Sasakawa H, Sugiharto B, O’Leary MH, Sugiyama T (1989) δ13C values in maize leaf correlate with phosphoenolpyruvate carboxylase levels. Plant Physiology 90, 582–585.
| δ13C values in maize leaf correlate with phosphoenolpyruvate carboxylase levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXksFCgt7k%3D&md5=a8de6fe0d3434882cc0d37e332000a3fCAS | 16666811PubMed |
Scoffoni C, Pou A, Aasamaa K, Sack L (2008) The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods. Plant, Cell & Environment 31, 1803–1812.
| The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods.Crossref | GoogleScholarGoogle Scholar |
Song Q, Zhang G, Zhu X-G (2013) Optimal crop canopy architecture to maximise canopy photosynthetic CO2 uptake under elevated CO2? A theoretical study using a mechanistic model of canopy photosynthesis. Functional Plant Biology 40, 108–124.
| Optimal crop canopy architecture to maximise canopy photosynthetic CO2 uptake under elevated CO2? A theoretical study using a mechanistic model of canopy photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1Knu74%3D&md5=02c79496fad505d78f3dd5edacefadb2CAS |
Tanaka Y, Sugano SS, Shimada T, Hara-Nishimura I (2013) Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytologist 198, 757–764.
| Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVykurw%3D&md5=41dfa517ce802702782ed59c1b9aa093CAS | 23432385PubMed |
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 & Environment 29, 691–700.
| Effects of growth light and nitrogen nutrition on the organization of the photosynthetic apparatus in leaves of a C4 plant, Amaranthus cruentus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xksl2msr0%3D&md5=eb4b82e166e8cf1948da196e92600518CAS |
Terashima I, Evans JR (1988) Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant & Cell Physiology 29, 143–155.
Tomás M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano H, Ribas-Carbó M, Tosens T, Vislap V, Niinemets Ü (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. Journal of Experimental Botany 64, 2269–2281.
| Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models.Crossref | GoogleScholarGoogle Scholar | 23564954PubMed |
Tosens T, Niinemets Ü, Westoby M, Wright IJ (2012) Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path. Journal of Experimental Botany 63, 5105–5119.
| Anatomical basis of variation in mesophyll resistance in eastern Australian sclerophylls: news of a long and winding path.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1ygsrfE&md5=9be1c3ad1a8d4ca19d87c92d00a98908CAS | 22888123PubMed |
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 |
Wang L, Czedik-Eysenberg A, Mertz RA, Si Y, Tohge T, Nunes-Nesi A, Arrivault S, Dedow LK, Bryant DW, Zhou W, Xu J, Weissmann S, Studer A, Li P, Zhang C, LaRue T, Shao Y, Ding Z, Sun Q, Patel RV, Turgeon R, Zhu X, Provart NJ, Mockler TC, Fernie AR, Stitt M, Liu P, Brutnell TP (2014) Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice. Nature Biotechnology 32, 1158–1165.
| Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice.Crossref | GoogleScholarGoogle Scholar | 25306245PubMed |
Warren CR (2008) Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. Journal of Experimental Botany 59, 1475–1487.
| Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlelt7w%3D&md5=75a7e1466915c1c5dc0880338fc0d92dCAS | 17975206PubMed |
Xiong D, Yu T, Zhang T, Li Y, Peng S, Huang J (2015) Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza. Journal of Experimental Botany 66, 741–748.
| Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza.Crossref | GoogleScholarGoogle Scholar | 25429002PubMed |
Yamori W, Nagai T, Makino A (2011) The rate-limiting step for CO2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species. Plant, Cell & Environment 34, 764–777.
| The rate-limiting step for CO2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVGks7k%3D&md5=9b9a94af897600357c68fbaea4d81eddCAS |