Rice (Oryza sativa) alleviates photosynthesis and yield loss by limiting specific leaf weight under low light intensity
Shoumik Saha A , Shampa Purkayastha A , Nimitha K A , Sebantee Ganguly A , Subhadeep Das A , Shamba Ganguly A , Nilanjan Sinha Mahapatra A , Kriti Bhattacharya A , Dibakar Das
A , Arup K. Saha A , Tirthankar Biswas A , Prabir K. Bhattacharyya A and Somnath Bhattacharyya A *
+ Author Affiliations
- Author Affiliations
A Department of Genetics and Plant Breeding, Crop Research Unit, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, PIN 741252, West Bengal, India.
* Correspondence to: somnathbhat@yahoo.com, bhattacharya.somnath@bckv.edu.in
Handling Editor: Suleyman Allakhverdiev
Functional Plant Biology 50(4) 267-276 https://doi.org/10.1071/FP22241
Submitted: 18 April 2022 Accepted: 11 December 2022 Published: 10 January 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The physiological mechanisms of shade tolerance and trait plasticity variations under shade remain poorly understood in rice (Oryza sativa L.). Twenty-five genotypes of rice were evaluated under open and shade conditions. Various parameters to identify variations in the plasticity of these traits in growth irradiance were measured. We found wide variations in specific leaf weight (SLW) and net assimilation rate measured at 400 µmol m−2 s−1 photosynthetic photon flux density (PPFD; referred to as A400) among the genotypes. Under shade, tolerant genotypes maintained a high rate of net photosynthesis by limiting specific leaf weight accompanied by increased intercellular CO2 concentration (Ci) compared with open-grown plants. On average, net photosynthesis was enhanced by 20% under shade, with a range of 2–30%. Increased accumulation of biomass under shade was observed, but it showed no correlation with photosynthetic plasticity. Chlorophyll a/b ratio also showed no association with photosynthetic rate and yield. Analysis of variance showed that 11%, 16%, and 37% of the total variance of A400, SLW, and Ci were explained due to differences in growth irradiance. SLW and A400 plasticity in growth irradiance was associated with yield loss alleviation with R2 values of 0.37 and 0.16, respectively. Biomass accumulation was associated with yield loss alleviation under shade, but no correlation was observed between A400 and leaf-N concentration. Thus, limiting specific leaf weight accompanied by increased Ci rather than leaf nitrogen concentration might have allowed rice genotypes to maintain a high net photosynthesis rate per unit leaf area and high yield under shade.
Keywords: intercellular CO2, leaf nitrogen concentration, low light, photosynthesis rate, plasticity, rice, specific leaf weight, yield.
References
Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany 32, 85–100.| A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants.Crossref | GoogleScholarGoogle Scholar |
Brestic M, Yang X, Li X, Allakhverdiev SI (2021) Crop photosynthesis for the twenty-first century. Photosynthesis Research 150, 1–3.
| Crop photosynthesis for the twenty-first century.Crossref | GoogleScholarGoogle Scholar |
Campany CE, Tjoelker MG, von Caemmerer S, Duursma RA (2016) Coupled response of stomatal and mesophyll conductance to light enhances photosynthesis of shade leaves under sunflecks. Plant, Cell & Environment 39, 2762–2773.
| Coupled response of stomatal and mesophyll conductance to light enhances photosynthesis of shade leaves under sunflecks.Crossref | GoogleScholarGoogle Scholar |
Carins Murphy MR, Jordan GJ, Brodribb TJ (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment 35, 1407–1418.
| Differential leaf expansion can enable hydraulic acclimation to sun and shade.Crossref | GoogleScholarGoogle Scholar |
Carins Murphy MR, Jordan GJ, Brodribb TJ (2014) Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant, Cell & Environment 37, 124–131.
| Acclimation to humidity modifies the link between leaf size and the density of veins and stomata.Crossref | GoogleScholarGoogle Scholar |
Carmo-Silva AE, Salvucci ME (2013) The regulatory properties of Rubisco activase differ among species and affect photosynthetic induction during light transitions. Plant Physiology 161, 1645–1655.
| The regulatory properties of Rubisco activase differ among species and affect photosynthetic induction during light transitions.Crossref | GoogleScholarGoogle Scholar |
Chen M, Luo J, Shao G, Wei X, Tang S, Sheng Z, Song J, Hu P (2012) Fine mapping of a major QTL for flag leaf width in rice, qFLW4, which might be caused by alternative splicing of NAL1. Plant Cell Reports 31, 863–872.
| Fine mapping of a major QTL for flag leaf width in rice, qFLW4, which might be caused by alternative splicing of NAL1.Crossref | GoogleScholarGoogle Scholar |
Chen L, Luo W, Huang J, Peng S, Xiong D (2021) Leaf photosynthetic plasticity does not predict biomass responses to growth irradiance in rice. Physiologia Plantarum 173, 2155–2165.
| Leaf photosynthetic plasticity does not predict biomass responses to growth irradiance in rice.Crossref | GoogleScholarGoogle Scholar |
Chowdhury PK, Thangaraj M, Jayapragasam M (1994) Biochemical changes in low-irradiance tolerant and susceptible rice cultivars. Biologia Plantarum 36, 237–242.
| Biochemical changes in low-irradiance tolerant and susceptible rice cultivars.Crossref | GoogleScholarGoogle Scholar |
Deng F, Li Q, Chen H, Zeng Y, Li B, Zhong X, et al. (2021) Relationship between chalkiness and the structural and thermal properties of rice starch after shading during grain-filling stage. Carbohydrate Polymers 252, 117212
| Relationship between chalkiness and the structural and thermal properties of rice starch after shading during grain-filling stage.Crossref | GoogleScholarGoogle Scholar |
Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell & Environment 24, 755–767.
| Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain.Crossref | GoogleScholarGoogle Scholar |
Fabre D, Adriani DE, Dingkuhn M, Ishimaru T, Punzalan B, Lafarge T, Clément-Vidal A, Luquet D (2016) The qTSN4 effect on flag leaf size, photosynthesis and panicle size, benefits to plant grain production in rice, depending on light availability. Frontiers in Plant Science 7, 623
| The qTSN4 effect on flag leaf size, photosynthesis and panicle size, benefits to plant grain production in rice, depending on light availability.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Wong SC (1984) An empirical model of stomatal conductance. Australian Journal of Plant Physiology 11, 191–210.
| An empirical model of stomatal conductance.Crossref | GoogleScholarGoogle Scholar |
Folini D, Wild M (2011) Aerosol emissions and dimming/brightening in Europe: sensitivity studies with ECHAM5-HAM. Journal of Geophysical Research: Atmospheres 116, D21104
| Aerosol emissions and dimming/brightening in Europe: sensitivity studies with ECHAM5-HAM.Crossref | GoogleScholarGoogle Scholar |
Fukao T, Yeung E, Bailey-Serres J (2012) The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice. Plant Physiology 160, 1795–1807.
| The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice.Crossref | GoogleScholarGoogle Scholar |
Ganguly S, Saha S, Vangaru S, Purkayastha S, Das D, Saha AK, Bhattacharyya S (2020) Identification and analysis of low light tolerant rice genotypes in field conditions and their SSR-based diversity in various abiotic stress tolerant lines. Journal of Genetics 99, 1–9.
| Identification and analysis of low light tolerant rice genotypes in field conditions and their SSR-based diversity in various abiotic stress tolerant lines.Crossref | GoogleScholarGoogle Scholar |
Hirota O, Oka M, Takeda T (1990) Sink activity estimation by sink size and dry matter increase during the ripening stage of barley (Hordeum vulgare) and rice (Oryza sativa). Annals of Botany 65, 349–353.
| Sink activity estimation by sink size and dry matter increase during the ripening stage of barley (Hordeum vulgare) and rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar |
Kaiser E, Kromdijk J, Harbinson J, Heuvelink E, Marcelis LFM (2017) Photosynthetic induction and its diffusional, carboxylation and electron transport processes as affected by CO2 partial pressure, temperature, air humidity and blue irradiance. Annals of Botany 119, 191–205.
| Photosynthetic induction and its diffusional, carboxylation and electron transport processes as affected by CO2 partial pressure, temperature, air humidity and blue irradiance.Crossref | GoogleScholarGoogle Scholar |
Lan Y, Woodrow IE, Mott KA (1992) Light-dependent changes in ribulose bisphosphate carboxylase activase activity in leaves. Plant Physiology 99, 304–309.
| Light-dependent changes in ribulose bisphosphate carboxylase activase activity in leaves.Crossref | GoogleScholarGoogle Scholar |
Li T, Yang Q (2015) Advantages of diffuse light for horticultural production and perspectives for further research. Frontiers in Plant Science 6, 704
| Advantages of diffuse light for horticultural production and perspectives for further research.Crossref | GoogleScholarGoogle Scholar |
Li Z, Pinson SRM, Stansel JW, Paterson AH (1998) Genetic dissection of the source-sink relationship affecting fecundity and yield in rice (shape Oryza sativa L.). Molecular Breeding 4, 419–426.
| Genetic dissection of the source-sink relationship affecting fecundity and yield in rice (shape Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Li X, Cai J, Li H, Bo Y, Liu F, Jiang D, Dai T, Cao W (2012) Effect of shading from jointing to maturity on high molecular weight glutenin subunit accumulation and glutenin macropolymer concentration in grain of winter wheat. Journal of Agronomy and Crop Science 198, 68–79.
| Effect of shading from jointing to maturity on high molecular weight glutenin subunit accumulation and glutenin macropolymer concentration in grain of winter wheat.Crossref | GoogleScholarGoogle Scholar |
Murchie EH, Hubbart S, Peng S, Horton P (2005) Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development. Journal of Experimental Botany 56, 449–460.
| Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development.Crossref | GoogleScholarGoogle Scholar |
Niinemets Ü, Keenan TF, Hallik L (2015) A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytologist 205, 973–993.
| A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types.Crossref | GoogleScholarGoogle Scholar |
Pearcy RW (1988) Photosynthetic utilisation of lightflecks by understory plants. Australian Journal of Plant Physiology 15, 223–238.
| Photosynthetic utilisation of lightflecks by understory plants.Crossref | GoogleScholarGoogle Scholar |
Pham VN, Kathare PK, Huq E (2018) Phytochromes and phytochrome interacting factors. Plant Physiology 176, 1025–1038.
| Phytochromes and phytochrome interacting factors.Crossref | GoogleScholarGoogle Scholar |
Pierik R, de Wit M (2014) Shade avoidance: phytochrome signalling and other aboveground neighbour detection cues. Journal of Experimental Botany 65, 2815–2824.
| Shade avoidance: phytochrome signalling and other aboveground neighbour detection cues.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Niinemets Ü, Ntagkas N, Siebenkäs A, Mäenpää M, Matsubara S, Pons TL (2019) A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytologist 223, 1073–1105.
| A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance.Crossref | GoogleScholarGoogle Scholar |
Rap A, Scott CE, Reddington CL, Mercado L, Ellis RJ, Garraway S, Evans MJ, Beerling DJ, MacKenzie AR, Hewitt CN, Spracklen DV (2018) Enhanced global primary production by biogenic aerosol via diffuse radiation fertilization. Nature Geoscience 11, 640–644.
| Enhanced global primary production by biogenic aerosol via diffuse radiation fertilization.Crossref | GoogleScholarGoogle Scholar |
Ren W-J, Yang W-Y, Xu J-W, Fan G-Q, Wang L-Y, Guan H (2002) Impact of lowlight stress on leaves characteristics of rice after heading. Journal of Sichuan Agricultural University 20, 205–208.
| Impact of lowlight stress on leaves characteristics of rice after heading.Crossref | GoogleScholarGoogle Scholar |
Schiferl LD, Heald CL (2018) Particulate matter air pollution may offset ozone damage to global crop production. Atmospheric Chemistry and Physics 18, 5953–5966.
| Particulate matter air pollution may offset ozone damage to global crop production.Crossref | GoogleScholarGoogle Scholar |
Scoffoni C, Kunkle J, Pasquet-Kok J, Vuong C, Patel AJ, Montgomery RA, et al. (2015) Light-induced plasticity in leaf hydraulics, venation, anatomy, and gas exchange in ecologically diverse Hawaiian lobeliads. New Phytologist 207, 43–58.
| Light-induced plasticity in leaf hydraulics, venation, anatomy, and gas exchange in ecologically diverse Hawaiian lobeliads.Crossref | GoogleScholarGoogle Scholar |
Shao L, Li G, Zhao Q, Li Y, Sun Y, Wang W, et al. (2020) The fertilization effect of global dimming on crop yields is not attributed to an improved light interception. Global Change Biology 26, 1697–1713.
| The fertilization effect of global dimming on crop yields is not attributed to an improved light interception.Crossref | GoogleScholarGoogle Scholar |
Shao L, Liu Z, Li H, Zhang Y, Dong M, Guo X, Zhang H, Huang B, Ni R, Li G, Cai C, Chen W, Luo W, Yin X (2021) The impact of global dimming on crop yields is determined by the source–sink imbalance of carbon during grain filling. Global Change Biology 27, 689–708.
| The impact of global dimming on crop yields is determined by the source–sink imbalance of carbon during grain filling.Crossref | GoogleScholarGoogle Scholar |
Tcherkez G (2013) Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters. Plant, Cell & Environment 36, 1586–1596.
| Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters.Crossref | GoogleScholarGoogle Scholar |
Tsukaguchi T, Tanaka R, Inoue H, Nakagawa H (2018) Effects of high temperature and shading on grain abscisic acid content and grain filling pattern in rice (Oryza sativa L.). Plant Production Science 21, 407–412.
| Effects of high temperature and shading on grain abscisic acid content and grain filling pattern in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Urban O, Janouš D, Acosta M, Czerný R, Marková I, Navrátil M, Pavelka M, Pokorný R, Šprtová M, Zhang R, Špunda V, Grace J, Marek MV (2007) Ecophysiological controls over the net ecosystem exchange of mountain spruce stand. Comparison of the response in direct vs. diffuse solar radiation. Global Change Biology 13, 157–168.
| Ecophysiological controls over the net ecosystem exchange of mountain spruce stand. Comparison of the response in direct vs. diffuse solar radiation.Crossref | GoogleScholarGoogle Scholar |
Vico G, Manzoni S, Palmroth S, Katul G (2011) Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes. New Phytologist 192, 640–652.
| Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes.Crossref | GoogleScholarGoogle Scholar |
Wang KC, Dickinson RE, Wild M, Liang S (2012) Atmospheric impacts on climatic variability of surface incident solar radiation. Atmospheric Chemistry and Physics 12, 9581–9592.
| Atmospheric impacts on climatic variability of surface incident solar radiation.Crossref | GoogleScholarGoogle Scholar |
Wang L, Deng F, Ren W-J (2015) Shading tolerance in rice is related to better light harvesting and use efficiency and grain filling rate during grain filling period. Field Crops Research 180, 54–62.
| Shading tolerance in rice is related to better light harvesting and use efficiency and grain filling rate during grain filling period.Crossref | GoogleScholarGoogle Scholar |
Wang X, Wu J, Chen M, Xu X, Wang Z, Wang B, Deng M (2018a) Field evidences for the positive effects of aerosols on tree growth. Global Change Biology 24, 4983–4992.
| Field evidences for the positive effects of aerosols on tree growth.Crossref | GoogleScholarGoogle Scholar |
Wang J, Lu K, Nie H, Zeng Q, Wu B, Qian J, Fang Z (2018b) Rice nitrate transporter OsNPF7.2 positively regulates tiller number and grain yield. Rice 11, 12
| Rice nitrate transporter OsNPF7.2 positively regulates tiller number and grain yield.Crossref | GoogleScholarGoogle Scholar |
Wei H-Y, Zhu Y, Qiu S, Han C, Hu L, Xu D, Zhou N-B, Xing Z-P, Hu Y-J, Cui P-Y, Dai Q-G, Zhang H-C (2018) Combined effect of shading time and nitrogen level on grain filling and grain quality in japonica super rice. Journal of Integrative Agriculture 17, 2405–2417.
| Combined effect of shading time and nitrogen level on grain filling and grain quality in japonica super rice.Crossref | GoogleScholarGoogle Scholar |
Wei H-H, Ge J-L, Zhang X-B, Zhu W, Deng F, Ren W-J, et al. (2022) Decreased panicle N application alleviates negative effects of shading on rice grain yield and grain quality. Journal of Integrative Agriculture
| Decreased panicle N application alleviates negative effects of shading on rice grain yield and grain quality.Crossref | GoogleScholarGoogle Scholar |
Xie X, Shan S, Wang Y, Cao F, Chen J, Huang M, Zou Y (2019) Dense planting with reducing nitrogen rate increased grain yield and nitrogen use efficiency in two hybrid rice varieties across two light conditions. Field Crops Research 236, 24–32.
| Dense planting with reducing nitrogen rate increased grain yield and nitrogen use efficiency in two hybrid rice varieties across two light conditions.Crossref | GoogleScholarGoogle Scholar |
Xin Q, Gong P, Suyker AE, Si Y (2016) Effects of the partitioning of diffuse and direct solar radiation on satellite-based modeling of crop gross primary production. International Journal of Applied Earth Observation and Geoinformation 50, 51–63.
| Effects of the partitioning of diffuse and direct solar radiation on satellite-based modeling of crop gross primary production.Crossref | GoogleScholarGoogle Scholar |
