Photosynthetica 2021, 59(4):496-507 | DOI: 10.32615/ps.2021.038

Effects of exposure of the leaf abaxial surface to direct solar radiation on the leaf anatomical traits and photosynthesis of soybean (Glycine max L.) in dryland farming systems

C. WANG1, Y.M. DU2, J.X. ZHANG1, J.T. REN1, P. HE3, T. WEI3, W. XIE3, H.K. YANG3, J.X. ZHANG1
1 College of Agriculture, Xinjiang Agricultural University, Urumqi, 830052 Xinjiang, China
2 Yili Institute of Agricultural Science, Yining, 835000 Xinjiang, China
3 Key Laboratory of Crop Eco-Physiology & Farming System in Southwest China, Sichuan Agriculture University, 611130 Chengdu, Sichuan Province, China

The frequent occurrence of monsoon winds usually leads to the formation of inverted soybean leaves. However, the effect of leaf inversion on photosynthetic capacity remains unclear. The responses of leaf anatomical traits, chlorophyll fluorescence induction kinetics parameters, photosynthetic capacity, and nonstructural carbohydrates of fully expanded leaves to inversion of leaves in two soybean cultivars were studied. Leaf inversion decreased the stomatal size and thickness of developed leaves. The net photosynthetic rate was significantly reduced under leaf inversion, which resulted from reduced excitation energy trapping and electron transport of PSII reaction center. Leaf inversion increased leaf temperature 10 d after leaf inversion but reduced the instantaneous water-use efficiency compared to normally oriented leaves. Due to the decreased light-saturated net photosynthetic rate, the soluble sugars of light-sensitive cultivar decreased significantly. In summary, leaf inversion deactivated the PSⅡ reaction centers, reduced photosynthesis and nonstructural carbohydrates in upper canopy soybean leaves.

Additional key words: carbohydrates; foliar anatomy traits; Glycine max (L.); light-response curves; photosynthesis.

Received: September 4, 2020; Revised: June 21, 2021; Accepted: July 7, 2021; Prepublished online: August 12, 2021; Published: December 17, 2021  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
WANG, C., DU, Y.M., ZHANG, J.X., REN, J.T., HE, P., WEI, T., ... ZHANG, J.X. (2021). Effects of exposure of the leaf abaxial surface to direct solar radiation on the leaf anatomical traits and photosynthesis of soybean (Glycine max L.) in dryland farming systems. Photosynthetica59(4), 496-507. doi: 10.32615/ps.2021.038
Download citation

References

  1. Aasamaa K., Aphalo P.J.: The acclimation of Tilia cordata stomatal opening in response to light, and stomatal anatomy to vegetational shade and its components. - Tree Physiol. 37: 209-219, 2017. Go to original source...
  2. Adamski J.M., Peters J.A., Danieloski R., Bacarin M.A.: Excess iron-induced changes in the photosynthetic characteristics of sweet potato. - J. Plant Physiol. 168: 2056-2062, 2011. Go to original source...
  3. Avola G., Cavallaro V., Patanè C., Giggi E.: Gas exchange and photosynthetic water use efficiency in response to light, CO2 concentration and temperature in Vicia faba. - J. Plant Physiol. 165: 796-804, 2008. Go to original source...
  4. Bahamonde H.A., Gil L., Fernández V.: Surface properties and permeability to calcium chloride of Fagus sylvatica and Quercus petraea leaves of different canopy heights. - Front. Plant Sci. 9: 494, 2018. Go to original source...
  5. Cai Y.P., Wang L.W., Chen L. et al.: Mutagenesis of GmFT2a and GmFT5a mediated by CRISPR/Cas9 contributes for expanding the regional adaptability of soybean. - Plant Biotechnol. J. 18: 298-309, 2020. Go to original source...
  6. Cao Y., Ding W.W., Zhang J.Z. et al.: Significant down-regulation of urea cycle generates clinically relevant proteomic signature in hepatocellular carcinoma patients with macrovascular invasion. - J. Proteome Res. 18: 2032-2044, 2019. Go to original source...
  7. Chen B.B., Zhang G.Y., Li P.H. et al.: Multiple GmWRI1s are redundantly involved in seed filling and nodulation by regulating plastidic glycolysis, lipid biosynthesis and hormone signalling in soybean (Glycine max). - Plant Biotechnol. J. 18: 155-171, 2020. Go to original source...
  8. Chen B.Y., Wang C.H., Tian Y.K. et al.: Anatomical characteristics of young stems and mature leaves of dwarf pear. - Sci. Hortic.-Amsterdam 186: 172-179, 2015. Go to original source...
  9. Couée I., Sulmon C., Gouesbet G. et al.: Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. - J. Exp. Bot. 57: 449-459, 2006. Go to original source...
  10. Dalberto D.S., Martinazzo E.G., Bacarin M.A.: Chlorophyll a fluorescence reveals adaptation strategies in drought stress in Ricinus communis. - Braz. J. Bot. 40: 861-870, 2017. Go to original source...
  11. Das R., Bhagawati K., Boro A. et al.: Relative performance of plant cultivars under respective water deficit adaptation strategies: A case study. - Curr. World Environ. 10: 683-690, 2015. Go to original source...
  12. Demmig-Adams B., Adams III W.W.: The role of xanthophyll cycle carotenoids in the protection of photosynthesis. - Trends Plant Sci. 1: 21-26, 1996. Go to original source...
  13. Durand M., Brendel O., Buré C., Le Thiec D.: Changes in irradiance and vapour pressure deficit under drought induce distinct stomatal dynamics between glasshouse and field grown poplars. - New Phytol. 227: 392-406, 2020. Go to original source...
  14. Düring H.: Stomatal and mesophyll conductances control CO2 transfer to chloroplasts in leaves of grapevine (Vitis vinifera L.). - Vitis 42: 65-68, 2003.
  15. Earles J.M., Buckley T.N., Brodersen C.R. et al.: Embracing 3D complexity in leaf carbon-water exchange. - Trends Plant Sci. 24: 15-24, 2019. Go to original source...
  16. Earles J.M., Guillaume T., Roddy A.B. et al.: Beyond porosity: 3D leaf intercellular airspace traits that impact mesophyll conductance. - Plant Physiol. 178: 148-162, 2018. Go to original source...
  17. Earles J.M., Théroux-Rancourt G., Gilbert M.E. et al.: Excess diffuse light absorption in upper mesophyll limits CO2 drawdown and depresses photosynthesis. - Plant Physiol. 174: 1082-1096, 2017. Go to original source...
  18. Ellsworth P.V., Ellsworth P.Z., Koteyeva N., Cousins A.B.: Cell wall properties in Oryza sativa influence mesophyll CO2 conductance. - New Phytol. 219: 66-76, 2018. Go to original source...
  19. Evans J.R.: Leaf anatomy enables more equal access to light and CO2 between chloroplasts. - New Phytol. 143: 93-104, 1999. Go to original source...
  20. Fanourakis D., Bouranis D., Giday H. et al.: Improving stomatal functioning at elevated growth air humidity: a review. - J. Plant Physiol. 207: 51-60, 2016. Go to original source...
  21. Fanourakis D., Hyldgaard B., Giday H. et al.: Stomatal anatomy and closing ability is affected by supplementary light intensity in rose (Rosa hybrida L.). - Hortic. Sci. 46: 81-89, 2019. Go to original source...
  22. Farquhar G.D., von Caemmerer S., Berry J.A.: Models of photosynthesis. - Plant Physiol. 125: 42-45, 2001. Go to original source...
  23. Feng L., Raza M.A., Li Z. et al.: The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of soybean. - Front. Plant Sci. 9: 1952, 2019. Go to original source...
  24. Flexas J., Cano F.J., Carriquí M. et al.: CO2 diffusion inside photosynthetic organs. - In: Adams III W.W., Terashima I. (ed.): The Leaf: A Platform for Performing Photosynthesis. Pp. 163-208. Springer, Cham 2018. Go to original source...
  25. Hao L.H., Guo L.L., Li R.Q. et al.: Responses of photosynthesis to high temperature stress associated with changes in leaf structure and biochemistry of blueberry (Vaccinium corymbosum L.). - Sci. Hortic.-Amsterdam 246: 251-264, 2019. Go to original source...
  26. Harrison E.L., Arce Cubas L., Gray J.E., Hepworth C.: The influence of stomatal morphology and distribution on photosynthetic gas exchange. - Plant J. 101: 768-779, 2020. Go to original source...
  27. Herrmann H.A., Schwartz J.-M., Johnson G.N.: From empirical to theoretical models of light response curves-linking photosynthetic and metabolic acclimation. - Photosynth. Res. 145: 5-14, 2020. Go to original source...
  28. Ichiro T., Hiroki O., Takashi F., Riichi O.: Light environment within a leaf. II. Progress in the past one-third century. - J. Plant Res. 129: 353-363, 2016. Go to original source...
  29. Iqbal N., Hussain S., Raza M.A. et al.: Drought tolerance of soybean (Glycine max L. Merr.) by improved photosynthetic characteristics and an efficient antioxidant enzyme system under a split-root system. - Front. Physiol. 10: 786, 2019. Go to original source...
  30. Isoda A., Mori M., Matsumoto S. et al.: High yielding performance of soybean in northern Xinjiang, China. - Plant Prod. Sci. 9: 401-407, 2006. Go to original source...
  31. Keunen E., Peshev D., Vangronsveld J. et al.: Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. - Plant Cell Environ. 36: 1242-1255, 2013. Go to original source...
  32. Kromdijk J., G³owacka K., Leonelli L. et al.: Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. - Science 354: 857-861, 2016. Go to original source...
  33. Lawson T., Vialet-Chabrand S.: Speedy stomata, photosynthesis and plant water use efficiency. - New Phytol. 221: 93-98, 2019. Go to original source...
  34. Li L., Shi Z.Y., Li L. et al.: Overexpression of ACL1 (abaxially curled leaf 1) increased bulliform cells and induced abaxial curling of leaf blades in rice. - Mol. Plant 3: 807-817, 2010. Go to original source...
  35. Li P.M., Fang P., Wang W.B. et al.: The higher resistance to chilling stress in adaxial side of Rumex K-1 leaves is accompanied with higher photochemical and non-photochemical quenching. - Photosynthetica 45: 496-502, 2007. Go to original source...
  36. Li Q.L., Mao H.P., Zuo Z.Y. et al.: Effects of nitrogen and phosphorus on the microstructure and ultrastructure of tomato leaves (Solanum lycopersicum). - J. Plant Nutr. 40: 1773-1783, 2017. Go to original source...
  37. Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987. Go to original source...
  38. Martin C.E., Hsu R., Lin T.C.: Comparative photosynthetic capacity of abaxial and adaxial leaf sides as related to exposure in two epiphytic ferns in a subtropical rainforest in Northeastern Taiwan. - Am. Fern J. 99: 145-154, 2009. Go to original source...
  39. Matthews J.S.A., Vialet-Chabrand S., Lawson T.: Acclimation to fluctuating light impacts the rapidity of response and diurnal rhythm of stomatal conductance. - Plant Physiol. 176: 1939-1951, 2018. Go to original source...
  40. Nazar R., Umar S., Khan N., Sareer O.: Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. - S. Afr. J. Bot. 98: 84-94, 2015. Go to original source...
  41. Pan J.Q., Guo B.L.: Effects of light intensity on the growth, photosynthetic characteristics, and flavonoid content of Epimedium pseudowushanense BL Guo. - Molecules 21: 1475, 2016. Go to original source...
  42. Pandey R., Chacko P.M., Choudhary M. et al.: Higher than optimum temperature under CO2 enrichment influences stomata anatomical characters in rose (Rosa hybrida). - Sci. Hortic.-Amsterdam 113: 74-81, 2007. Go to original source...
  43. Paradiso R., de Visser P.H.B., Arena C., Marcelis L.F.M.: Light response of photosynthesis and stomatal conductance of rose leaves in the canopy profile: the effect of lighting on the adaxial and the abaxial sides. - Funct. Plant Biol. 47: 639-650, 2020. Go to original source...
  44. Paradiso R., Marcelis L.F.M.: The effect of irradiating adaxial or abaxial side on photosynthesis of rose leaves. - Acta Hortic. 956: 157-163, 2012. Go to original source...
  45. Pires M.V., Almeida A.-A.F., Figueiredo A.L. et al.: Photosynthetic characteristics of ornamental passion flowers grown under different light intensities. - Photosynthetica 49: 593-602, 2011. Go to original source...
  46. Proietti P., Palliotti A.: Contribution of the adaxial and abaxial surfaces of olive leaves to photosynthesis. - Photosynthetica 33: 63-69, 1997. Go to original source...
  47. Richardson F., Brodribb T.J., Jordan G.J.: Amphistomatic leaf surfaces independently regulate gas exchange in response to variations in evaporative demand. - Tree Physiol. 37: 869-878, 2017. Go to original source...
  48. Ruiz-Vera U.M., Siebers M., Gray S.B. et al.: Global warming can negate the expected CO2 stimulation in photosynthesis and productivity for soybean grown in the midwestern United States. - Plant Physiol. 162: 410-423, 2013. Go to original source...
  49. Sefton C.A., Montagu K., Atwell B.J., Conroy J.P.: Anatomical variation in juvenile eucalypt leaves accounts for differences in specific leaf area and CO2 assimilation rates. - Aust. J. Bot. 50: 301-310, 2002. Go to original source...
  50. Singh M., Kumar J., Singh S. et al.: Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. - Rev. Environ. Sci. Biotechnol. 14: 407-426, 2015. Go to original source...
  51. Soares-Cordeiro A.S., Driscoll S.P., Arrabaça M.C., Foyer C.H.: Dorsoventral variations in dark chilling effects on photosynthesis and stomatal function in Paspalum dilatatum leaves. -J. Exp. Bot. 62: 687-699, 2011. Go to original source...
  52. Tamagno S., Sadras V.O., Ortez O.A., Ciampitti I.A.: Allometric analysis reveals enhanced reproductive allocation in historical set of soybean varieties. - Field Crop. Res. 248: 107717, 2020. Go to original source...
  53. Terashima I., Hanba Y.T., Tazoe Y. et al.: Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. - J. Exp. Bot. 57: 343-354, 2006. Go to original source...
  54. Terashima I., Hanba Y.T., Tholen D., Niinemets Ü.: Leaf functional anatomy in relation to photosynthesis. - Plant Physiol. 155: 108-116, 2011. Go to original source...
  55. Thalmann M., Santelia D.: Starch as a determinant of plant fitness under abiotic stress. - New Phytol. 214: 943-951, 2017. Go to original source...
  56. Tian S.F., Guo R.Z., Zou X.X. et al.: Priming with the green leaf volatile (Z)-3-hexeny-1-yl acetate enhances salinity stress tolerance in peanut (Arachis hypogaea L.) seedlings. - Front. Plant Sci. 10: 785, 2019. Go to original source...
  57. Turner N.C., Singh D.P.: Responses of adaxial and abaxial stomata to light and water deficits in sunflower and sorghum. -New Phytol. 96: 187-195, 1984. Go to original source...
  58. Verboven P., Herremans E., Helfen L. et al.: Synchrotron X-ray computed laminography of the three-dimensional anatomy of tomato leaves. - Plant J. 81: 169-182, 2015. Go to original source...
  59. Voelker S.L., Brooks J.R., Meinzer F.C. et al.: A dynamic leaf gas-exchange strategy is conserved in woody plants under changing ambient CO2: evidence from carbon isotope discrimination in paleo and CO2 enrichment studies. - Glob. Change Biol. 22: 889-902, 2016. Go to original source...
  60. Wang Y., Noguchi K., Terashima I.: Distinct light responses of the adaxial and abaxial stomata in intact leaves of Helianthus annuus L. - Plant Cell Environ. 31: 1307-1316, 2008. Go to original source...
  61. Wang Y., Noguchi K., Terashima I.: Photosynthesis-dependent and -independent responses of stomata to blue, red and green monochromatic light: differences between the normally oriented and inverted leaves of sunflower. - Plant Cell Physiol. 52: 479-489, 2011. Go to original source...
  62. Wang Z.T., Sun Z.Q., Lu S.: Optimal vegetation index for assessing leaf water potential using reflectance factors from the adaxial and abaxial surfaces. - Comput. Electron. Agr. 172: 105337, 2020. Go to original source...
  63. Wen K.J., Liang C.J., Wang L.H. et al.: Combined effects of lanthanumion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings. - Chemosphere 84: 601-608, 2011. Go to original source...
  64. Wu Y.S., Gong W.Z., Yang W.Y.: Shade inhibits leaf size by controlling cell proliferation and enlargement in soybean. - Sci. Rep.-UK 7: 9259, 2017. Go to original source...
  65. Xiong D.L., Douthe C., Flexas J.: Differential coordination of stomatal conductance, mesophyll conductance, and leaf hydraulic conductance in response to changing light across species. - Plant Cell Environ. 41: 436-450, 2018. Go to original source...
  66. Xu W.Z., Deng X.P., Xu B.C: Effects of water stress and fertilization on leaf gas exchange and photosynthetic light-response curves of Bothriochloa ischaemum L. - Photosynthetica 51: 603-612, 2013. Go to original source...
  67. Yan Y.H., Wan Y., Liu W.G. et al.: Influence of seed treatment with uniconazole powder on soybean growth, photosynthesis, dry matter accumulation after flowering and yield in relay strip intercropping system. - Plant Prod. Sci. 18: 295-301, 2015. Go to original source...
  68. Yang F., Feng L.Y., Liu Q.L. et al.: Effect of interactions between light intensity and red-to-far-red ratio on the photosynthesis of soybean leaves under shade condition. - Environ. Exp. Bot. 150: 79-87, 2018. Go to original source...
  69. Yang H.K., Wu G., Mo P. et al.: The combined effects of maize straw mulch and no-tillage on grain yield and water and nitrogen use efficiency of dryland winter wheat (Triticum aestivum L.). - Soil Till. Res. 197: 104485, 2020. Go to original source...
  70. Yang H.K., Zhang X.Y., Chen B.L. et al.: Integrated management strategies increase cottonseed, oil and protein production: the key role of carbohydrate metabolism. - Front. Plant Sci. 8: 48, 2017. Go to original source...
  71. Yao X.D., Li C.H., Li S.Y. et al.: Effect of shade on leaf photosynthetic capacity, light-intercepting, electron transfer and energy distribution of soybeans. - Plant Growth Regul. 83: 409-416, 2017. Go to original source...
  72. Yu H.Y., Murchie E.H., González-Carranza Z.H. et al.: Decreased photosynthesis in the erect panicle 3 (ep3) mutant of rice is associated with reduced stomatal conductance and attenuated guard cell development. - J. Exp. Bot. 66: 1543-1552, 2015. Go to original source...
  73. Yusuf M.A., Kumar D., Rajwanshi R. et al.: Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: Physiological and chlorophyll a fluorescence measurements. - BBA-Bioenergetics 1797: 1428-1438, 2010. Go to original source...
  74. Zhang Z.S., Li Y.T., Gao H.Y. et al.: Characterization of photosynthetic gas exchange in leaves under simulated adaxial and abaxial surfaces alternant irradiation. - Sci. Rep.-UK 6: 26963, 2016. Go to original source...