Acclimation strategy and plasticity of different soybean genotypes in intercropping
Sajad Hussain
A B , Ting Pang A B , Nasir Iqbal C , Iram Shafiq A B , Milan Skalicky D , Marian Brestic D E , Muhammad E. Safdar F , Maryam Mumtaz A , Aftab Ahmad A B , Muhammad A. Asghar A B , Ali Raza A B , Suleyman I. Allakhverdiev G H I J K L , Yi Wang A B , Xiao C. Wang A B , Feng Yang A B , Taiwen Yong A B , Weiguo Liu A B M and Wenyu Yang A B M
+ Author Affiliations
- Author Affiliations
A College of Agronomy, Sichuan Agricultural University, 211-Huimin Road, Wenjiang District,Chengdu 611130, PR China.
B Sichuan Engineering Research Center for Crop Strip Intercropping System, Key Laboratory of Crop Ecophysiology and Farming System in Southwest China (Ministry of Agriculture), Sichuan Agricultural University, Chengdu, PR China.
C School of Agriculture, Food and Wine, The University of Adelaide, Waite Campus, Urrbrae, SA 5064, Australia.
D Department of Botany and Plant Physiology, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, 165 00 Prague, Czech Republic.
E Department of Plant Physiology, Slovak University of Agriculture, 94976 Nitra, Slovakia.
F College of Agriculture, University of Sargodha, Sargodha, Pakistan.
G K.A. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, Moscow 127276, Russia.
H Institute of Basic Biological Problems, Russian Academy of Sciences, Institutskaya Street 2, Pushchino, Moscow Region 142290, Russia.
I Department of Plant Physiology, Faculty of Biology, MV Lomonosov Moscow State University, Leninskie Gory 1-12, Moscow 119991, Russia.
J Institute of Molecular Biology and Biotechnology, Azerbaijan National Academy of Sciences, Matbuat Avenue 2a, Baku 1073, Azerbaijan.
K College of Science, King Saud University, Riyadh, Saudi Arabia.
L Department of Molecular and Cell Biology, Moscow Institute of Physics and Technology, Institutsky lane 9, Dolgoprudny, Moscow region 141700, Russia.
M Corresponding authors. Email: lwgsy@126.com; mssiyangwy@sicau.edu.cn
Functional Plant Biology 47(7) 592-610 https://doi.org/10.1071/FP19161
Submitted: 4 June 2019 Accepted: 18 December 2019 Published: 7 May 2020
Abstract
In response to shading, plant leaves acclimate through a range of morphological, physiological and biochemical changes. Plants produce a myriad of structurally and functionally diverse metabolites that play many important roles in plant response to continually changing environmental conditions as well as abiotic and biotic stresses. To develop a clearer understanding of the effects of shade on soybeans at different growth stages, a comprehensive, three-year, stage-wise study was conducted. Leaf area, leaf thickness, stem diameter, chlorophyll contents, photosynthetic characteristics and other morphological and physiological features were measured along with biochemical assays for antioxidants such as superoxide dismutase, peroxidase and caralase and yield attributes of different soybean genotypes (Guixia 2, Nandou12, Nandong Kang-22, E61 and C103) under shading nets with 50% light transmittance. It was observed that early shading (VER1 and VER2) significantly decreased main stem length and main stem length/stem diameter. Later shading (R1R8 and R2R8) had significant effects on morphological characters such as branch number and pod height. In Nandou 12, the protein contents in plants shaded at R1R8, R2R8 and R5R8 were 9.20, 8.98 and 6.23% higher than in plants grown under normal light levels (CK), respectively, and the crude fat content was 9.31, 10.74 and 4.28% lower. The influence of shading in the later period on anatomy was greater than that in the earlier period. Shading reduced the light saturation point (LSP), the light compensation point (LCP) and the maximum photosynthetic rate (Pnmax), and increased the apparent quantum yield (AQ). Shading also increased the antioxidant enzyme activity in the plants, and this increase was greater with early shading than late. The variability in the chlorophyll (a + b) content and the chlorophyll a/b ratio in R2 stage plants was less than in R5 stage (VER5) plants. Similarly, the activity of antioxidant enzymes in R2 after returning the plants to normal light levels (VER2) was lower than in R5 after relighting (VER5). Compared with later shading, the early shading had a greater effect on the photosynthetic and related characteristics. The longer the shading time, the greater the adverse effects and the less able the plants’ were to recover. The data collected in this study contribute to an understanding of the physiological mechanisms underlying the early and late growth stage acclimation strategies in different soybean genotypes subjected to shade stress.
Additional keywords: antioxidants, photosynthetic, proteins, shading, soybean, yield.
References
Ali MB, Hahn E-J, Paek K-Y (2005) Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet. Environmental and Experimental Botany 54, 109–120.| Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet.Crossref | GoogleScholarGoogle Scholar |
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
| Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 15377225PubMed |
Artru S, Dumont B, Ruget F, Launay M, Ripoche D, Lassois L, Garré) S (2018) How does STICS crop model simulate crop growth and productivity under shade conditions? Field Crops Research 215, 83–93.
| How does STICS crop model simulate crop growth and productivity under shade conditions?Crossref | GoogleScholarGoogle Scholar |
Bianculli ML, Aguirrezábal LA, Irujo GAP, Echarte MM (2016) Contribution of incident solar radiation on leaves and pods to soybean seed weight and composition. European Journal of Agronomy 77, 1–9.
| Contribution of incident solar radiation on leaves and pods to soybean seed weight and composition.Crossref | GoogleScholarGoogle Scholar |
Board JE (1987) Yield components related to seed yield in determinate soybean. Crop Science 27, 1296–1297.
| Yield components related to seed yield in determinate soybean.Crossref | GoogleScholarGoogle Scholar |
Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2004) Plasticity in light reactions of photosynthesis for energy production and photoprotection. Journal of Experimental Botany 56, 395–406.
| Plasticity in light reactions of photosynthesis for energy production and photoprotection.Crossref | GoogleScholarGoogle Scholar | 15533877PubMed |
Dai Y, Shen Z, Liu Y, Wang L, Hannaway D, Lu H (2009) Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environmental and Experimental Botany 65, 177–182.
| Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg.Crossref | GoogleScholarGoogle Scholar |
Dong S, Jiang Y, Dong Y, Wang L, Wang W, Ma Z, Yan C, Ma C, Liu L (2019) A study on soybean responses to drought stress and rehydration. Saudi Journal of Biological Sciences 26, 2006–2017.
| A study on soybean responses to drought stress and rehydration.Crossref | GoogleScholarGoogle Scholar | 31889786PubMed |
Du C-H, Liu T-X, Jiang H-T, Li C-H (2011) Effects of low light stress and light recovery on reactive oxygen metabolism of maize seedlings. Journal of Nuclear Agricultural Sciences 3, 570–575.
Fan Y, Chen J, Cheng Y, Raza MA, Wu X, Wang Z, Liu Q, Wang R, Wang X, Yong T, Liu W, Liu J, Du J, Shu K, Yang W, Yang F (2018) Effect of shading and light recovery on the growth, leaf structure, and photosynthetic performance of soybean in a maize–soybean relay-strip intercropping system. PLoS One 13, e0198159
| Effect of shading and light recovery on the growth, leaf structure, and photosynthetic performance of soybean in a maize–soybean relay-strip intercropping system.Crossref | GoogleScholarGoogle Scholar | 30379963PubMed |
Fan Y, Chen J, Wang Z, Tan T, Li S, Li J, Wang B, Zhang J, Cheng Y, Wu X, Yang W, Yang F (2019) Soybean (Glycine max L. Merr.) seedlings response to shading: leaf structure, photosynthesis and proteomic analysis. BMC Plant Biology 19, 34
| Soybean (Glycine max L. Merr.) seedlings response to shading: leaf structure, photosynthesis and proteomic analysis.Crossref | GoogleScholarGoogle Scholar | 30665369PubMed |
Feng L, Raza MA, Li Z, Chen Y, Khalid MHB, Du J, Liu W, Wu X, Song C, Yu L (2018) The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of soybean. Frontiers of Plant Science 9, 1952
| The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of soybean.Crossref | GoogleScholarGoogle Scholar |
Fenollosa E, Munné-Bosch S (2018) Photoprotection and photo-oxidative stress markers as useful tools to unravel plant invasion success. In ‘Advances in plant ecophysiology techniques’. pp. 153–175. (Springer: Berlin)
García’-Plazaola JI, Becerril JM, Hernández A, Niinemets Ü, Kollist H (2004) Acclimation of antioxidant pools to the light environment in a natural forest canopy. New Phytologist 163, 87–97.
| Acclimation of antioxidant pools to the light environment in a natural forest canopy.Crossref | GoogleScholarGoogle Scholar |
Gaudio N, Escobar-Gutiérrez AJ, Casadebaig P, Evers JB, Gérard F, Louarn G, Colbach N, Munz S, Launay M, Marrou H (2019) Current knowledge and future research opportunities for modeling annual crop mixtures. A review. Agronomy for Sustainable Development 39, 20
| Current knowledge and future research opportunities for modeling annual crop mixtures. A review.Crossref | GoogleScholarGoogle Scholar |
Green-Tracewicz E, Page ER, Swanton CJ (2011) Shade avoidance in soybean reduces branching and increases plant-to-plant variability in biomass and yield per plant. Weed Science 59, 43–49.
| Shade avoidance in soybean reduces branching and increases plant-to-plant variability in biomass and yield per plant.Crossref | GoogleScholarGoogle Scholar |
Hussain S, Iqbal N, Brestic M, Raza MA, Pang T, Langham DR, Safdar ME, Ahmed S, Wen B, Gao Y, Liu W, Yang W (2019a) Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment. Science of the Total Environment 658, 626–637.
| Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment.Crossref | GoogleScholarGoogle Scholar | 30580217PubMed |
Hussain S, Iqbal N, Rahman T, Liu T, Brestic M, Safdar ME, Asghar MA, Farooq MU, Shafiq I, Ali A, Shoaib M, Chen G, Qin S, Liu W, Yang W (2019b) Shade effect on carbohydrates dynamics and stem strength of soybean genotypes. Environmental and Experimental Botany 162, 374–382.
| Shade effect on carbohydrates dynamics and stem strength of soybean genotypes.Crossref | GoogleScholarGoogle Scholar |
Hussain S, Iqbal N, Ting P, Khan MN, Liu W-G, Yang W-Y (2019c) Weak stem under shade reveals the lignin reduction behavior. Journal of Integrative Agriculture 18, 496–505.
| Weak stem under shade reveals the lignin reduction behavior.Crossref | GoogleScholarGoogle Scholar |
Hussain S, Liu T, Iqbal N, Brestic M, Pang T, Mumtaz M, Shafiq I, Li S, Wang L, Gao Y, Khan A, Ahmad I, Allakhverdiev SI, Liu W, Yang W (2020) Effects of lignin, cellulose, hemicellulose, sucrose and monosaccharide carbohydrates on soybean physical stem strength and yield in intercropping. Photochemical & Photobiological Sciences.
| Effects of lignin, cellulose, hemicellulose, sucrose and monosaccharide carbohydrates on soybean physical stem strength and yield in intercropping.Crossref | GoogleScholarGoogle Scholar |
Iqbal N, Hussain S, Ahmed Z, Yang F, Wang X, Liu W, Yong T, Du J, Shu K, Yang W (2018) Comparative analysis of maize–soybean strip intercropping systems: a review. Plant Production Science 22, 131–142.
| Comparative analysis of maize–soybean strip intercropping systems: a review.Crossref | GoogleScholarGoogle Scholar |
Islam MT, Kubota F, Mollah MFH, Agata W (1993) Effect of shading on the growth and yield of mungbean (Vigna radiata (L.) Wilczek). Journal Agronomy & Crop Science 171, 274–278.
| Effect of shading on the growth and yield of mungbean (Vigna radiata (L.) Wilczek).Crossref | GoogleScholarGoogle Scholar |
James A, Lawn R (2011) Application of physiological understanding in soybean improvement. II. Broadening phenological adaptation across regions and sowing dates. Crop and Pasture Science 62, 12–24.
| Application of physiological understanding in soybean improvement. II. Broadening phenological adaptation across regions and sowing dates.Crossref | GoogleScholarGoogle Scholar |
Kantolic AG, Peralta GE, Slafer GA (2013) Seed number responses to extended photoperiod and shading during reproductive stages in indeterminate soybean. European Journal of Agronomy 51, 91–100.
| Seed number responses to extended photoperiod and shading during reproductive stages in indeterminate soybean.Crossref | GoogleScholarGoogle Scholar |
Keuskamp DH, Sasidharan R, Vos I, Peeters AJM, Voesenek LACJ, Pierik R (2011) Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings. The Plant Journal 67, 208
| Blue-light-mediated shade avoidance requires combined auxin and brassinosteroid action in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 21457374PubMed |
Kumudini S, Omielan J, Hume D (2008) Soybean genetic improvement in yield and the effect of late-season shading and nitrogen source and supply. Agronomy Journal 100, 400–405.
| Soybean genetic improvement in yield and the effect of late-season shading and nitrogen source and supply.Crossref | GoogleScholarGoogle Scholar |
Kunzheng C, Shiming L (1999) Effect of shading on growth, development and yield formation of rice. Chinese Journal of Applied Ecology 17, 657–662.
Liu W, Deng Y, Hussain S, Zou J, Yuan J, Luo L, Yang C, Yuan X, Yang W (2016) Relationship between cellulose accumulation and lodging resistance in the stem of relay intercropped soybean (Glycine max (L.) Merr.). Field Crops Research 196, 261–267.
| Relationship between cellulose accumulation and lodging resistance in the stem of relay intercropped soybean (Glycine max (L.) Merr.).Crossref | GoogleScholarGoogle Scholar |
Liu X, Rahman T, Song C, Su B, Yang F, Yong T, Wu Y, Zhang C, Yang W (2017) Changes in light environment, morphology, growth and yield of soybean in maize–soybean intercropping systems. Field Crops Research 200, 38–46.
| Changes in light environment, morphology, growth and yield of soybean in maize–soybean intercropping systems.Crossref | GoogleScholarGoogle Scholar |
Liu W-g, Ren M-l, Liu T, Du Y-l, Zhou T, Liu X-m, Liu J, Hussain S, Yang W-y (2018a) Effect of shade stress on lignin biosynthesis in soybean stems. Journal of Integrative Agriculture 17, 1594–1604.
| Effect of shade stress on lignin biosynthesis in soybean stems.Crossref | GoogleScholarGoogle Scholar |
Liu X, Rahman T, Song C, Yang F, Su B, Cui L, Bu W, Yang W (2018b) Relationships among light distribution, radiation use efficiency and land equivalent ratio in maize-soybean strip intercropping. Field Crops Research 224, 91–101.
| Relationships among light distribution, radiation use efficiency and land equivalent ratio in maize-soybean strip intercropping.Crossref | GoogleScholarGoogle Scholar |
Liu YJ, Zhang W, Wang ZB, Ma L, Guo YP, Ren XL, Mei LX (2019) Influence of shading on photosynthesis and antioxidative activities of enzymes in apple trees. Photosynthetica 57, 857–865.
| Influence of shading on photosynthesis and antioxidative activities of enzymes in apple trees.Crossref | GoogleScholarGoogle Scholar |
Nico M, Miralles DJ, Kantolic AG (2015) Post-flowering photoperiod and radiation interaction in soybean yield determination: direct and indirect photoperiodic effects. Field Crops Research 176, 45–55.
| Post-flowering photoperiod and radiation interaction in soybean yield determination: direct and indirect photoperiodic effects.Crossref | GoogleScholarGoogle Scholar |
Peña’-Valdivia CB, Ortega’-Delgado ML (1991) Non’-structural carbohydrate partitioning in Phaseolus vulgaris after vegetative growth. Journal of the Science of Food and Agriculture 55, 563–577.
| Non’-structural carbohydrate partitioning in Phaseolus vulgaris after vegetative growth.Crossref | GoogleScholarGoogle Scholar |
Puglielli G, Crescente MF, Frattaroli AR, Gratani L (2015) Morphological, anatomical and physiological leaf trait plasticity of Sesleria nitida (Poaceae) in open vs shaded conditions. Polish Journal of Ecology 63, 10–22.
| Morphological, anatomical and physiological leaf trait plasticity of Sesleria nitida (Poaceae) in open vs shaded conditions.Crossref | GoogleScholarGoogle Scholar |
Qi-hua L, Xue-biao Z, Lian-qun Y, Tian L, Jian-jun Z (2009) Effects of early growth stage shading on rice flag leaf physiological characters and grain growth at grain-filling stage. Chinese Journal of Applied Ecology 20, 2135–2141.
Quevedo-Rojas A, García-Núñez C, Jerez-Rico M, Jaimez R, Schwarzkopf T (2018) Leaf acclimation strategies to contrasting light conditions in saplings of different shade tolerance in a tropical cloud forest. Functional Plant Biology 45, 968–982.
| Leaf acclimation strategies to contrasting light conditions in saplings of different shade tolerance in a tropical cloud forest.Crossref | GoogleScholarGoogle Scholar | 32291060PubMed |
Silva EN, Silveira JA, Aragão RM, Vieira CF, Carvalho FE (2019) Photosynthesis impairment and oxidative stress in Jatropha curcas exposed to drought are partially dependent on decreased catalase activity. Acta Physiologiae Plantarum 41, 4
| Photosynthesis impairment and oxidative stress in Jatropha curcas exposed to drought are partially dependent on decreased catalase activity.Crossref | GoogleScholarGoogle Scholar |
Sterck FJ, Duursma RA, Pearcy RW, Valladares F, Cieslak M, Weemstra M (2013) Plasticity influencing the light compensation point offsets the specialization for light niches across shrub species in a tropical forest understorey. Journal of Ecology 101, 971–980.
| Plasticity influencing the light compensation point offsets the specialization for light niches across shrub species in a tropical forest understorey.Crossref | GoogleScholarGoogle Scholar |
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology Evolution and Systematics 39, 237–257.
| Shade tolerance, a key plant feature of complex nature and consequences.Crossref | GoogleScholarGoogle Scholar |
Van Roekel RJ, Purcell LC, Salmerón M (2015) Physiological and management factors contributing to soybean potential yield. Field Crops Research 182, 86–97.
| Physiological and management factors contributing to soybean potential yield.Crossref | GoogleScholarGoogle Scholar |
Wu Y, Gong W, Yang W (2017) Shade inhibits leaf size by controlling cell proliferation and enlargement in soybean. Scientific Reports 7, 9259
| Shade inhibits leaf size by controlling cell proliferation and enlargement in soybean.Crossref | GoogleScholarGoogle Scholar | 28835715PubMed |
Wu Y, Gong W, Wang Y, Yong T, Yang F, Liu W, Wu X, Du J, Shu K, Liu J (2018) Leaf area and photosynthesis of newly emerged trifoliolate leaves are regulated by mature leaves in soybean. Journal of Plant Research 131, 671–680.
| Leaf area and photosynthesis of newly emerged trifoliolate leaves are regulated by mature leaves in soybean.Crossref | GoogleScholarGoogle Scholar | 29600314PubMed |
Xianzhao L, Shaozhong K (2002) Effects of shading on photosynthesis and yield of tomato plants at different growth stages. Acta Horticulturae Sinica 29, 427–432.
Yang F, Huang S, Gao R, Liu W, Yong T, Wang X, Wu X, Yang W (2014) Growth of soybean seedlings in relay strip intercropping systems in relation to light quantity and red : far-red ratio. Field Crops Research 155, 245–253.
| Growth of soybean seedlings in relay strip intercropping systems in relation to light quantity and red : far-red ratio.Crossref | GoogleScholarGoogle Scholar |
Yao X, Li C, Li S, Zhu Q, Zhang H, Wang H, Yu C, St Martin SK, Xie F (2017) Effect of shade on leaf photosynthetic capacity, light-intercepting, electron transfer and energy distribution of soybeans. Plant Growth Regulation 83, 409–416.
| Effect of shade on leaf photosynthetic capacity, light-intercepting, electron transfer and energy distribution of soybeans.Crossref | GoogleScholarGoogle Scholar |
Zhang J, Dong S, Wang K, Hu C, Liu P (2007) Effects of shading in field on photosynthetic characteristics in summer corn. CBA 636796
Zhang Y, Liu A, Huang S (2018) Effects of shading on some morphological and physiological characteristics of Begonia semperflorens. Pakistan Journal of Botany 50, 2173–2179.
Zhu H, Li X, Zhai W, Liu Y, Gao Q, Liu J, Ren L, Chen H, Zhu Y (2017) Effects of low light on photosynthetic properties, antioxidant enzyme activity, and anthocyanin accumulation in purple pak-choi (Brassica campestris ssp. Chinensis Makino). PLoS One 12, e0179305
| Effects of low light on photosynthetic properties, antioxidant enzyme activity, and anthocyanin accumulation in purple pak-choi (Brassica campestris ssp. Chinensis Makino).Crossref | GoogleScholarGoogle Scholar | 29240840PubMed |
Zivcak M, Brestic M, Kalaji HM (2014) Photosynthetic responses of sun-and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynthesis Research 119, 339–354.
| Photosynthetic responses of sun-and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light?Crossref | GoogleScholarGoogle Scholar | 24445618PubMed |
