Photosynthesis Research

, Volume 137, Issue 2, pp 183–200 | Cite as

Co-regulation of photosynthetic processes under potassium deficiency across CO2 levels in soybean: mechanisms of limitations and adaptations

  • Shardendu K. SinghEmail author
  • Vangimalla R. Reddy
Original Article


Plants photosynthesis-related traits are co-regulated to capture light and CO2 to optimize the rate of CO2 assimilation (A). The rising CO2 often benefits, but potassium (K) deficiency adversely affects A that contributes to the majority of plant biomass. To evaluate mechanisms of photosynthetic limitations and adaptations, soybean was grown under controlled conditions with an adequate (control, 5.0 mM) and two K-deficient (moderate, 0.50 and severe, 0.02 mM) levels under ambient (aCO2; 400 µmol mol−1) and elevated CO2 (eCO2; 800 µmol mol−1). Results showed that under severe K deficiency, pigments, leaf absorption, processes of light and dark reactions, and CO2 diffusion through stomata and mesophyll were down co-regulated with A while light compensation point increased and photorespiration, alternative electron fluxes, and respiration were up-regulated. However, under moderate K deficiency, these traits were well co-regulated with the sustained A without any obvious limitations amid ≈ 50% reduction in leaf K level. Primary mechanism of K limitation to A was either biochemical processes (Lb ≈ 60%) under control and moderate K deficiency or the CO2 diffusion limitations (DL ≈ 70%) with greater impacts of mesophyll than stomatal pathways under severe K deficiency. The eCO2 increased DL while lessened the Lb under K deficiency. Adaptation strategies to severe K deficiency included an enhanced K utilization efficiency (KUE), and reduction of photosystem II excitation pressure by decreasing photosynthetic pigments, light absorption, and photochemical quenching while increasing photorespiration and alternative electron fluxes. The eCO2 also stimulated A and KUE when K deficiency was not severe. Thus, plants responded to K deficiency by a coordinated regulation of photosynthetic processes to optimize A, and eCO2 failed to alleviate the DL in severely K-deficient plants.


Alternative electron sink Carboxylation CO2 diffusion Glycine max Photochemistry Photorespiration 



The CO2 assimilation rate


Gross CO2 assimilation rate (i.e., A + RdYin)


The A obtained at the Imax beyond which there is no significant change in A


The curve referring to the A response to the Ci


The curve referring to the A response to PAR


Standardized A as estimated at ≈ 400 µmol mol−1 Ci


Ambient or external CO2 concentration


Sub-stomatal CO2 concentration


Chloroplastic CO2 concentration


Diffusional limitation (i.e., Ls + Lm)


Quantum efficiency by oxidized (open) PSII reaction center in light


Stomatal conductance


Mesophyll conductance


Potential rate of electron transport to support NADP + reduction for RuBP regeneration


The alternative electron flux as the proportion of total electron fluxes (i.e., [(JFJG)/JF] × 100)


Fluorescence-based electron transport rate or total electron flux (i.e., s × PAR × ΦPSII)


Gas exchange-based electron transport rate (i.e., AG × 4 under NPR)




Potassium utilization efficiency


Light compensation point


Light saturation point

Ls, Lm, Lb

Stomatal, mesophyll, and biochemical limitations, respectively


Non-photorespiratory conditions (i.e., photosynthetic measurement using 2% O2)


Photosynthetically active radiation


Photosynthetic carbon reduction


Photorespiratory carbon oxidation


Photosystem II


Photochemical quenching


Dark respiration in the light


Day respiration (i.e., respiratory CO2 release other than by photorespiration) as estimated under NPR condition using Yin et al. (2009, 2011) method


Ribulose-1,5-bisphosphate carboxylase/oxygenase




The parameter referring to the leaf absorptance of incident PAR by photosynthetic pigments and excitation partitioning to PSII


Total chlorophyll concentration


Triose phosphate utilization


Maximal rate of carboxylation

\({\Phi _{{\text{C}}{{\text{O}}_{\text{2}}}}}\)

Quantum yield of CO2 fixation (i.e., A + RdYin/PAR)


Quantum yield of CO2 fixation at PAR 200 µmol m−2 s−1 (i.e., form the initial slope of the A/PAR curve)


Photochemical yield of PSII electron transport rate



The authors thank Mr. Darryl Baxam (Engineering Technician) and Jackson Fisher (Biological Science) for the help in maintaining the growth chambers and measurements, and Ms. Mariam Manzoor and Shruti Bhatt (undergraduate students) for providing assistance during the experiment.

Supplementary material

11120_2018_490_MOESM1_ESM.docx (121 kb)
Supplementary material 1 (DOCX 121 KB)


  1. Ahmed FE, Hall AE, Madore MA (1993) Interactive effects of high temperature and elevated carbon dioxide concentration on cowpea (Vigna unguiculata (L.) Walp.). Plant Cell Environ 16:835–842CrossRefGoogle Scholar
  2. Andrews AK, Svec LV (1976) Pod and leaf photosynthesis and disease incidence in soybean (Glycine max (L.) Merr.) with potassium fertilization. Commun Soil Sci Plant Anal 7:345–363CrossRefGoogle Scholar
  3. Battie-Laclau P, Laclau J-P, Beri C, Mietton L, Muniz MRA, Arenque BC, De Cassia Piccolo M, Jordan-Meille L, Bouillet J-P, Nouvellon Y (2014) Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant Cell Environ 37:70–81CrossRefPubMedGoogle Scholar
  4. Bednarz CW, Oosterhuis DM (1999) Physiological changes associated with potassium deficiency in cotton. J Plant Nutr 22:303–313CrossRefGoogle Scholar
  5. Bednarz CW, Oosterhuis DM, Evans RD (1998) Leaf photosynthesis and carbon isotope discrimination of cotton in response to potassium deficiency. Environ Exp Bot 39:131–139CrossRefGoogle Scholar
  6. Bernacchi CJ, Morgan PB, Ort DR, Long SP (2005) The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220:434–446CrossRefPubMedGoogle Scholar
  7. Bunce J (2002) Sensitivity of infrared water vapor analyzers to oxygen concentration and errors in stomatal conductance. Photosynth Res 71:273–276CrossRefPubMedGoogle Scholar
  8. Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530CrossRefGoogle Scholar
  9. Cakmak I, Hengeler C, Marschner H (1994) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250CrossRefGoogle Scholar
  10. Ciha AJ, Brun WA (1975) Stomatal size and frequency in soybeans. Crop Sci 15:309–313CrossRefGoogle Scholar
  11. Cooper RB, Blaser RE, Brown RH (1967) Potassium nutrition effects on net photosynthesis and morphology of alfalfa. Soil Sci Soc Am J 31:231–235CrossRefGoogle Scholar
  12. Durchan M, Vácha F, Krieger-Liszkay A (2001) Effects of severe CO2 starvation on the photosynthetic electron transport chain in tobacco plants. Photosynth Res 68:203CrossRefPubMedGoogle Scholar
  13. Edwards GE, Baker NR (1993) Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis? Photosynth Res 37:89–102CrossRefPubMedGoogle Scholar
  14. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345CrossRefGoogle Scholar
  15. Farquhar GD, Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90CrossRefPubMedGoogle Scholar
  16. Flexas J, Bota J, Escalona JM, Sampol B, Medrano H (2002) Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Funct Plant Biol 29:461–471CrossRefGoogle Scholar
  17. Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henkle M, Martínez-Cañellas S, Medrano H (2006) Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytol 172:73–82CrossRefPubMedGoogle Scholar
  18. Flexas J, Ribas-Carbó M, Díaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621CrossRefPubMedGoogle Scholar
  19. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  20. Gerardeaux E, Saur E, Constantin J, Porté A, Jordan-Meille L (2009) Effect of carbon assimilation on dry weight production and partitioning during vegetative growth. Plant Soil 324:329–343CrossRefGoogle Scholar
  21. Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol 99:1443–1448CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hanway JJ, Weber CR (1971) N, P, and K percentages in soybean (Glycine max (L.) Merrill) plant parts. Agron J 63:286–290CrossRefGoogle Scholar
  23. Hewitt EJ (1952) Sand and Water Culture. Methods used in the study of plant nutrition. Technical Communication No. 22. Commonwealth Bureau of Horticulture and Plantation, East Malling, Maidstone, Kent. Commonwealth Agricultural Bureaux Farmham Royal, Bucks, pp 187–190Google Scholar
  24. Huber SC (1984) Biochemical basis for effects of K-deficiency on assimilate export rate and accumulation of soluble sugars in soybean leaves. Plant Physiol 76:424–430CrossRefPubMedPubMedCentralGoogle Scholar
  25. Humble GD, Raschke K (1971) Stomatal opening quantitatively related to potassium transport: evidence from electron probe analysis. Plant Physiol 48:447–453CrossRefPubMedPubMedCentralGoogle Scholar
  26. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change [Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds)]. Cambridge University Press, CambridgeGoogle Scholar
  27. Ivanov A, Hurry V, Sane P, Öquist G, Huner NA (2008) Reaction centre quenching of excess light energy and photoprotection of photosystem II. J Plant Biol 51:85–96CrossRefGoogle Scholar
  28. Jákli B, Tavakol E, Tränkner M, Senbayram M, Dittert K (2017) Quantitative limitations to photosynthesis in K deficient sunflower and their implications on water-use efficiency. J Plant Physiol 209:20–30CrossRefPubMedGoogle Scholar
  29. Jin SH, Huang JQ, Li XQ, Zheng BS, Wu JS, Wang ZJ, Liu GH, Chen M (2011) Effects of potassium supply on limitations of photosynthesis by mesophyll diffusion conductance in Carya cathayensis. Tree Physiol 31:1142–1151CrossRefPubMedGoogle Scholar
  30. Laisk A, Loreto F (1996) Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence (ribulose-1,5-bisphosphate carboxylase/oxygenase specificity factor, dark respiration in the light, excitation distribution between photosystems, alternative electron transport rate, and mesophyll diffusion resistance). Plant Physiol 110:903–912CrossRefPubMedPubMedCentralGoogle Scholar
  31. Larbi A, Abadía A, Abadía J, Morales F (2006) Down co-regulation of light absorption, photochemistry, and carboxylation in Fe-deficient plants growing in different environments. Photosynth Res 89:113–126CrossRefPubMedGoogle Scholar
  32. Lenka NK, Lal R (2012) Soil-related constraints to the carbon dioxide fertilization effect. Crit Rev Plant Sci 31:342–357CrossRefGoogle Scholar
  33. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthesis. Methods Enzymol 148:350–352CrossRefGoogle Scholar
  34. Lobo FdA, de Barros MP, Dalmagro HJ, Dalmolin ÂC, Pereira WE, de Souza ÉC, Vourlitis GL, Rodríguez Ortíz CE (2013) Fitting net photosynthetic light-response curves with Microsoft Excel—a critical look at the models. Photosynthetica 51:445–456CrossRefGoogle Scholar
  35. Loreto F, Di Marco G, Tricoli D, Sharkey T (1994) Measurements of mesophyll conductance, photosynthetic electron transport and alternative electron sinks of field grown wheat leaves. Photosynth Res 41:397–403CrossRefPubMedGoogle Scholar
  36. Lu Z, Lu J, Pan Y, Lu P, Li X, Cong R, Ren T (2016a) Anatomical variation of mesophyll conductance under potassium deficiency has a vital role in determining leaf photosynthesis. Plant Cell Environ 39:2428–2439CrossRefPubMedGoogle Scholar
  37. Lu Z, Ren T, Pan Y, Li X, Cong R, Lu J (2016b) Differences on photosynthetic limitations between leaf margins and leaf centers under potassium deficiency for Brassica napus L. Sci Rep 6:21725CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ma Q, Scanlan C, Bell R, Brennan R (2013) The dynamics of potassium uptake and use, leaf gas exchange and root growth throughout plant phenological development and its effects on seed yield in wheat (Triticum aestivum) on a low-K sandy soil. Plant Soil 373:373–384CrossRefGoogle Scholar
  39. Miyake C (2010) Alternative electron flows (water–water cycle and cyclic electron flow around psi) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963CrossRefPubMedGoogle Scholar
  40. Ort DR (2001) When there is too much light. Plant Physiol 125:29–32CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198CrossRefPubMedGoogle Scholar
  42. Ozbun JL, Volk RJ, Jackson WA (1965) Effect of potassium deficiency on photosynthesis, respiration and the utilization of photosynthetic reductant by immature bean leaves. Crop Sci 5:69–75CrossRefGoogle Scholar
  43. Peoples TR, Koch DW (1979) Role of potassium in carbon dioxide assimilation in Medicago sativa L. Plant Physiol 63:878–881CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pérez-López U, Robredo A, Lacuesta M, Mena-Petite A, Muñoz-Rueda A (2012) Elevated CO2 reduces stomatal and metabolic limitations on photosynthesis caused by salinity in Hordeum vulgare. Photosynth Res 111:269–283CrossRefPubMedGoogle Scholar
  45. Prioul JL, Chartier P (1977) Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used. Ann Bot 41:789–800CrossRefGoogle Scholar
  46. Reddy KR, Zhao DL (2005) Interactive effects of elevated CO2 and potassium deficiency on photosynthesis, growth, and biomass partitioning of cotton. Field Crops Res 94:201–213CrossRefGoogle Scholar
  47. Römheld V, Kirkby E (2010) Research on potassium in agriculture: needs and prospects. Plant Soil 335:155–180CrossRefGoogle Scholar
  48. Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368CrossRefPubMedGoogle Scholar
  49. Saxton AM (1998) A macro for converting mean separation output to letter groupings in Proc Mixed. In: Proceedings of the 23rd SAS users group international. SAS Institute, CaryGoogle Scholar
  50. Shabala S (2003) Regulation of potassium transport in leaves: from molecular to tissue level. Ann Bot 92:627–634CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040CrossRefPubMedGoogle Scholar
  52. Siddiqi MY, Glass ADM (1981) Utilization index: a modified approach to the estimation and comparison of nutrient utilization efficiency in plants. J Plant Nutr 4:289–302CrossRefGoogle Scholar
  53. Singh SK, Reddy VR (2014) Combined effects of phosphorus nutrition and elevated carbon dioxide concentration on chlorophyll fluorescence, photosynthesis and nutrient efficiency of cotton. J Plant Nutr Soil Sci 177:892–902CrossRefGoogle Scholar
  54. Singh SK, Reddy VR (2015) Response of carbon assimilation and chlorophyll fluorescence to soybean leaf phosphorus across CO2: alternative electron sink, nutrient efficiency and critical concentration. J Photochem Photobiol B 151:276–284CrossRefPubMedGoogle Scholar
  55. Singh SK, Reddy VR (2016) Methods of mesophyll conductance estimation: its impact on key biochemical parameters and photosynthetic limitations in phosphorus stressed soybean across CO2. Physiol Plant 157:234–254CrossRefPubMedGoogle Scholar
  56. Singh SK, Reddy VR (2017) Potassium starvation limits soybean growth more than the photosynthetic processes across CO2 levels. Front Plant Sci 8:991CrossRefPubMedPubMedCentralGoogle Scholar
  57. Singh SK, Badgujar G, Reddy VR, Fleisher DH, Bunce JA (2013) Carbon dioxide diffusion across stomata and mesophyll and photo-biochemical processes as affected by growth CO2 and phosphorus nutrition in cotton. J Plant Physiol 170:801–813CrossRefPubMedGoogle Scholar
  58. Singh SK, Reddy VR, Fleisher HD, Timlin JD (2014) Growth, nutrient dynamics, and efficiency responses to carbon dioxide and phosphorus nutrition in soybean. J Plant Int 9:838–849Google Scholar
  59. Singh SK, Reddy VR, Sharma MP, Agnihotri R (2015) Dynamics of plant nutrients, utilization and uptake, and soil microbial community in crops under ambient and elevated carbon dioxide. In: Rakshit A, Singh HB, Sen A (eds) Nutrient use efficiency: from basics to advances. Springer, New Delhi, pp 381–399CrossRefGoogle Scholar
  60. Taiz L, Zeiger E, Møller IM, Murphy A (2014) Plant physiology and development. Sinauer Associates, Inc, SunderlandGoogle Scholar
  61. Van Kooten O, Snel FHJ (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150CrossRefPubMedGoogle Scholar
  62. Warren CR, Ethier GJ, Livingston NJ, Grant NJ, Turpin DH, Harrison DL, Black TA (2003) Transfer conductance in second growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) canopies. Plant Cell Environ 26:1215–1227CrossRefGoogle Scholar
  63. Weis E, Berry JA (1987) Quantum efficiency of photosystem II in relation to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochim Biophys Acta 894:198–208CrossRefGoogle Scholar
  64. Weng X-Y, Zheng C-J, Xu H-X, Sun J-Y (2007) Characteristics of photosynthesis and functions of the water–water cycle in rice (Oryza sativa) leaves in response to potassium deficiency. Physiol Plant 131:614–621CrossRefPubMedGoogle Scholar
  65. Yi X-P, Zhang Y-L, Yao H-S, Zhang X-J, Luo H-H, Gou L, Zhang W-F (2014) Alternative electron sinks are crucial for conferring photoprotection in field-grown cotton under water deficit during flowering and boll setting stages. Funct Plant Biol 41:737–747CrossRefGoogle Scholar
  66. Yin X, Struik PC, Romero P, Harbinson J, Evers JB, Van Der Putten PEL, Vos JAN (2009) Using combined measurements of gas exchange and chlorophyll fluorescence to estimate parameters of a biochemical C3 photosynthesis model: a critical appraisal and a new integrated approach applied to leaves in a wheat (Triticum aestivum) canopy. Plant Cell Environ 32:448–464CrossRefPubMedGoogle Scholar
  67. Yin X, Sun Z, Struik PC, Gu J (2011) Evaluating a new method to estimate the rate of leaf respiration in the light by analysis of combined gas exchange and chlorophyll fluorescence measurements. J Exp Bot 62:3489–3499CrossRefPubMedPubMedCentralGoogle Scholar
  68. Zhao D, Oosterhuis DM, Bednarz CW (2001) Influence of potassium deficiency on photosynthesis, chlorophyll content, and chloroplast ultrastructure of cotton plants. Photosynthetica 39:103–109CrossRefGoogle Scholar

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© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018

Authors and Affiliations

  1. 1.Adaptive Cropping Systems LaboratoryUSDA-ARSBeltsvilleUSA
  2. 2.Wye Research and Education CenterUniversity of MarylandCollege ParkUSA

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