Advertisement

Photosynthesis in Poor Nutrient Soils, in Compacted Soils, and under Drought

  • Fermín MoralesEmail author
  • Andrej Pavlovič
  • Anunciación Abadía
  • Javier Abadía
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)

Summary

Plants require the uptake of nutrients (in most cases via roots) and their incorporation into plant organs for growth. In non-woody species, 83% of fresh weight is water, 7% is carbon, 5% is oxygen, with the remaining 5% including hydrogen and such nutrients. In natural ecosystems, availability of nutrients in soils is heterogeneous, and many species often adapt their growth to the amount of nutrients that roots can take up by exploring the available soil volume. In agricultural areas, the lack of some nutrients is frequent. In both cases, plants must also face periods of drought and soil compaction. These environmental stresses are therefore not uncommon in natural ecosystems and crops, and the stressed plants often experience a decrease in photosynthetic CO2 fixation. In this chapter, we review changes observed in photosynthesis in response to nutrient deficiencies, soil compaction, and drought. The current knowledge on photosynthesis in carnivorous plants, as a special case of plant species growing in nutrient poor soils, is also included. Pigment limitations (chlorosis and/or necrosis), stomatal limitations, ultrastructural effects and mesophyll conductance limitations, photochemistry (primary reactions), carboxylation and Calvin-cycle reactions, and carbohydrate metabolism and transport will be discussed. With regard to nutrients, we have focused on the most common nutrition-related stresses in plants, the deficiencies of macro- (nitrogen, phosphorous, and potassium) and micronutrients (iron, manganese, copper, and zinc). Other nutrient deficiencies (or toxicities, both in the cases of essential nutrient excess or heavy metals) are not reviewed here. For other nutrient deficiencies and toxicities, and the role of the above-mentioned, and other nutrients (such as calcium and magnesium) in gas exchange, and as intracellular signal transducers, enzyme activators, and structure and function stabilizers of biological membranes, readers are referred to papers published elsewhere (Marschner H, Mineral nutrition of higher plants. Academic, London, 1995; Cakmak I, Kirkby EA, Physiol Plant 133:692–704, 2008; Morales F, Warren CR, Photosynthetic responses to nutrient deprivation and toxicities. In: Flexas J, Loreto F, Medrano H (eds) Terrestrial photosynthesis in a changing environment: a molecular, physiological and ecological approach. Cambridge University Press, Cambridge, pp 312–330, 2012; Hochmal AK, Schulze S, Trompelt K, Hippler M, Biochim Biophys Acta 1847:993–1003, 2015).

Abbreviations

Al

aluminum

Amax

maximum rate of light-saturated photosynthesis

AOX

alternative oxidase

ATP

adenosine triphosphate

B

boron

Ca

calcium

Cd

cadmium

Chl

chlorophyll

Ci

concentration of CO2 in the leaf mesophyll tissue

Cu

copper

DM

dry mass

Fe

iron

K

potassium

Mg

magnesium

Mo

molybdenum

Mn

manganese

N

nitrogen

Na

sodium

P

phosphorous

Pi

inorganic P

PNUE

photosynthetic N use efficiency

PS

photosystem

Rubisco

ribulose bisphosphate carboxylase-oxygenase

RuBP

ribulose-1,5-bisphosphate

WUE

water use efficiency

Zn

zinc

Notes

Acknowledgements

This study was supported by the Spanish Ministry of Economy and Competitiveness (MINECO; projects AGL2012-31988, AGL2013-42175-R, AGL2016-75226-R, and AGL2016-79868-R, co-financed with FEDER), the Aragón Government (Group A03), grant LO1204 (Sustainable development of research in the Centre of the Region Haná) from the National Program of Sustainability I, and by the Czech Science Foundation Agency (project 16-07366Y). FM wishes to thank JC Martínez for his help with some periodic bibliographic searches.

References

  1. Abadía J, Nishio JN, Terry N (1986) Chlorophyll-protein and polypeptide composition of Mn-deficient sugar beet thylakoids. Photosynth Res 7:379–381CrossRefGoogle Scholar
  2. Adamec L (2003) Zero water flow in the carnivorous genus Genlisea. Carniv Plant Newsl 32:46–48Google Scholar
  3. Adamec L (2006) Respiration and photosynthesis of bladders and leaves of aquatic Utricularia species. Plant Biol 8:765–769PubMedCrossRefGoogle Scholar
  4. Adamec L (2008) The influence of prey capture on photosynthetic rate in two aquatic carnivorous plant species. Aquat Bot 89:66–70CrossRefGoogle Scholar
  5. Adamec L (2010) Dark respiration of leaves and traps of terrestrial carnivorous plants: are there greater energetic costs in traps? Cent Eur J Biol 5:121–124Google Scholar
  6. Adamec L (2012) Firing and resetting characteristics of carnivorous Utricularia reflexa traps: physiological or only physical regulation of trap triggering. Phyton 52:281–290Google Scholar
  7. Agbariah K-T, Roth-Bejerano N (1990) The effect of blue light on energy levels in epidermal strips. Physiol Plant 78:100–104CrossRefGoogle Scholar
  8. Ahmed M, Qadeer U, Ahmed ZI, Fayyaz-ul H (2016) Improvement of wheat (Triticum aestivum) drought tolerance by seed priming with silicon. Arch Agron Soil Sci 62:299–315CrossRefGoogle Scholar
  9. Al-Abbas AH, Barr R, Hall JD, Crane FL, Baumgardner MF (1974) Spectra of normal and nutrient deficient maize leaves. Agron J 66:16–20CrossRefGoogle Scholar
  10. Andrade A, Wolfe DW, Fereres E (1993) Leaf expansion, photosynthesis, and water relations of sunflower plants grown on compacted soil. Plant Soil 149:175–184CrossRefGoogle Scholar
  11. Arquero O, Barranco D, Benlloch M (2006) Potassium starvation increases stomatal conductance in olive trees. Hortscience 41:433–436Google Scholar
  12. Arshad M, Ali S, Noman A, Ali Q, Rizwan M, Farid M, Irshad MK (2016) Phosphorus amendment decreased cadmium (Cd) uptake and ameliorates chlorophyll contents, gas exchange attributes, antioxidants, and mineral nutrients in wheat (Triticum aestivum L.) under Cd stress. Arch Agron Soil Sci 62:533–546CrossRefGoogle Scholar
  13. Arulanantham A, Rao I, Terry N (1990) Limiting factors in photosynthesis. VI. Regeneration of ribulose 1,5-bisphosphate limits photosynthesis at low photochemical capacity. Plant Physiol 93:1466–1475PubMedPubMedCentralCrossRefGoogle Scholar
  14. Barón M, Arellano JB, López Gorgé J (1995) Copper and photosystem II: a controversial relationship. Physiol Plant 94:174–180CrossRefGoogle Scholar
  15. Basile B, Reidel EJ, Weinbaum SA, DeJong TM (2003) Leaf potassium concentration, CO2 exchange and light interception in almond trees (Prunus dulcis (Mill) D.A. Webb). Sci Hortic 98:185–194CrossRefGoogle Scholar
  16. Baszynski T, Wajda L, Krol M, Wolinska D, Krupa Z, Tukendorf A (1980) Photosynthetic activities of cadmium-treated tomato plants. Physiol Plant 48:365–370CrossRefGoogle Scholar
  17. Bazile V, Le Moguédec G, Marshall DJ, Gaume L (2015) Fluid physico-chemical properties influence capture and diet in Nepenthes pitcher plants. Ann Bot 115:705–716PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bhattarai SP, Huber S, Midmore DJ (2004) Aerated subsurface irrigation water gives growth and yield benefits to Zucchini, vegetable soybean and cotton in heavy clay soils. Ann Appl Biol 144:285–298CrossRefGoogle Scholar
  19. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252CrossRefGoogle Scholar
  20. Bohn HF, Federle W (2004) Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. Proc Natl Acad Sci USA 101:14138–14143PubMedCrossRefGoogle Scholar
  21. Bottrill DE, Possingham JV, Kriedemann PE (1970) The effect of nutrient deficiencies on photosynthesis and respiration in spinach. Plant Soil 32:424–438CrossRefGoogle Scholar
  22. Bown HE, Watt MS, Clinton PW, Mason EG, Whitehead D (2009) The influence of N and P supply and genotype on carbon flux and partitioning in potted Pinus radiata plants. Tree Physiol 29:1143–1151PubMedCrossRefGoogle Scholar
  23. Brooks A (1986) Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin cycle metabolites in spinach leaves. Aust J Plant Physiol 13:221–237CrossRefGoogle Scholar
  24. Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704PubMedCrossRefGoogle Scholar
  25. Carrasco-Gil S, Rios JJ, Álvarez-Fernández A, Abadía A, García-Mina JM, Abadía J (2016) Effects of individual and combined metal foliar fertilization on iron- and manganese-deficient Solanum lycopersicum plants. Plant Soil 402:27–45CrossRefGoogle Scholar
  26. Chen WR, Yang X, He ZL, Feng Y, Hu FH (2008) Differential changes in photosynthetic capacity, 77 K chlorophyll fluorescence and chloroplast ultrastructure between Zn-efficient and Zn-inefficient rice genotypes (Oryza sativa) under low zinc stress. Physiol Plant 132:89–101PubMedCrossRefGoogle Scholar
  27. Coley PD (1988) Effects of plant-growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–536CrossRefGoogle Scholar
  28. Colombi T, Walter A (2016) Root responses of triticale and soybean to soil compaction in the field are reproducible under controlled conditions. Funct Plant Biol 43:114–128CrossRefGoogle Scholar
  29. Conlin TSS, van den Driessche R (1996) Short term effects of soil compaction on growth of Pinus contorta seedlings. Can J For Res 26:727–739CrossRefGoogle Scholar
  30. Costa-e-Silva F, Correia AC, Piayda A, Dubbert M, Rebmann C, Cuntz M, Werner C, David JS, Pereira JS (2015) Effects of an extremely dry winter on net ecosystem carbon exchange and tree phenology at a cork oak woodland. Agric For Meteorol 204:48–57CrossRefGoogle Scholar
  31. Cruz JL, Mosquim PR, Pelacani CR, Araujo WL, Da Matta FM (2003) Photosynthesis impairment in cassava leaves in response to nitrogen deficiency. Plant Soil 257:417–423CrossRefGoogle Scholar
  32. Da Matta FM, Maestri M, Barros RS (1997) Photosynthetic performance of two coffee species under drought. Photosynthetica 34:257–264CrossRefGoogle Scholar
  33. Dahal K, Martyn GD, Vanlerberghe GC (2015) Improved photosynthetic performance during severe drought in Nicotiana tabacum overexpressing a nonenergy conserving respiratory electron sink. New Phytol 208:382–395PubMedCrossRefGoogle Scholar
  34. Dixon KW, Pate JS, Bailey WJ (1980) Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. with special reference to catch of arthropod fauna by its glandular leaves. Aust J Bot 28:283–297CrossRefGoogle Scholar
  35. Dubey RS (1997) Photosynthesis in plants under stressful conditions. In: Pessarakli M (ed) Handbook of photosynthesis. Marcel Dekker Inc, New York, pp 859–875Google Scholar
  36. Ellison AM (2006) Nutrient limitation and stoichiometry of carnivorous plants. Plant Biol 8:740–747PubMedCrossRefGoogle Scholar
  37. Ellison AM, Adamec L (2011) Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same? Oikos 120:1721–1731CrossRefGoogle Scholar
  38. Ellison AM, Farnsworth EJ (2005) The cost of carnivory for Darlingtonia californica (Sarraceniaceae): evidence from relationships among leaf traits. Am J Bot 92:1085–1093PubMedCrossRefGoogle Scholar
  39. Ellison AM, Gotelli NJ (2001) Evolutionary ecology of carnivorous plants. Trends Ecol Evol 16:623–629CrossRefGoogle Scholar
  40. Ellison AM, Gotelli NJ (2002) Nitrogen availability alters the expression of carnivory in the northern pitcher plant, Sarracenia purpurea. Proc Natl Acad Sci USA 99:4409–4412PubMedCrossRefGoogle Scholar
  41. Erel R, Yermiyahu U, Ben-Gal A, Dag A, Shapira O, Schwartz A (2015) Modification of non-stomatal limitation and photoprotection due to K and Na nutrition of olive trees. J Plant Physiol 177:1–10PubMedCrossRefGoogle Scholar
  42. Escalante-Pérez M, Krol E, Stange A, Geiger D, Al-Rasheid KA, Hause B, Neher E, Hedrich R (2011) A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap. Proc Natl Acad Sci USA 108:15492–15497PubMedCrossRefGoogle Scholar
  43. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  44. Evans JR, Terashima I (1987) Effects of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14:59–68CrossRefGoogle Scholar
  45. Farnsworth EJ, Ellison AM (2008) Prey availability directly affects physiology, growth, nutrient allocation and scaling relationships among leaf traits in 10 carnivorous plant species. J Ecol 96:213–221Google Scholar
  46. Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624PubMedCrossRefGoogle Scholar
  47. Ferrar PJ, Osmond CB (1986) Nitrogen supply as a factor influencing photoinhibition and photosynthetic acclimation after transfer of shade-grown Solanum dulcamara to bright light. Planta 168:563–570PubMedCrossRefGoogle Scholar
  48. Ferree DC, Streeter JG (2004) Response of container-grown grapevines to soil compaction. Hortsci 39:1250–1254Google Scholar
  49. Ferree DC, Streeter JG, Yuncong Y (2004) Response of container-grown apple trees to soil compaction. Hortsci 39:40–48Google Scholar
  50. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of form and function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  51. Field C, Merino J, Mooney HA (1983) Compromises between water-use efficiency and nitrogen-use efficiency in 5 species of California evergreens. Oecologia 60:384–389PubMedCrossRefGoogle Scholar
  52. Filek M, Łabanowska M, Kościelniak J, Biesaga-Kościelniak J, Kurdziel M, Szarejko I, Hartikainen H (2015) Characterization of barley leaf tolerance to drought stress by chlorophyll fluorescence and electron paramagnetic resonance studies. J Agron Crop Sci 201:228–240CrossRefGoogle Scholar
  53. Flaig H, Mohr H (1992) Assimilation of nitrate and ammonium by the Scots pine (Pinus sylvestris) seedling under conditions of high nitrogen supply. Physiol Plant 84:568–576CrossRefGoogle Scholar
  54. Flexas J, Medrano H (2002) Energy dissipation in C3 plants under drought. Funct Plant Biol 29:1209–1215CrossRefGoogle Scholar
  55. Flexas J, Escalona JM, Medrano H (1999) Water stress induces different levels of photosynthesis and electron transport rate regulation in grapevines. Plant Cell Environ 22:39–48CrossRefGoogle Scholar
  56. Flexas J, Bota J, Escalona JM, Sampól 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
  57. Flores RA, Borges BMMN, Almeida HR, Prado RDM (2015) Growth and nutritional disorders of eggplant cultivated in nutrient solutions with suppressed macronutrients. J Plant Nutr 38:1097–1109CrossRefGoogle Scholar
  58. Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol 89:225–230PubMedPubMedCentralCrossRefGoogle Scholar
  59. Frydenvang J, van Maarschalkerweerd M, Carstensen A, Mundus S, Schmidt SB, Pedas PR, Laursen KH, Schjoerring JK, Husted S (2015) Sensitive detection of phosphorus deficiency in plants using chlorophyll a fluorescence. Plant Physiol 169:353–361PubMedPubMedCentralCrossRefGoogle Scholar
  60. Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiol 116:571–580PubMedPubMedCentralCrossRefGoogle Scholar
  61. Fu CX, Li M, Zhang Y, Zhang YZ, Yan YJ, Wang YA (2015) Morphology, photosynthesis, and internal structure alterations in field apple leaves under hidden and acute zinc deficiency. Sci Hortic 193:47–54CrossRefGoogle Scholar
  62. Fukushima K, Fujita H, Yamaguchi T, Kawaguchi M, Tsukaya H, Hasebe M (2015) Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea. Nat Commun 6:6450PubMedPubMedCentralCrossRefGoogle Scholar
  63. Galmés J, Kapralov MV, Andralojc PJ, Conesa MÀ, Keys AJ, Parry MAJ, Flexas J (2014) Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends. Plant Cell Environ 37:1989–2001PubMedCrossRefGoogle Scholar
  64. Gates DM (1970) Physical and physiological properties of plants. In: Remote sensing. National Academy of Sciences, Washington DC, pp 224–252Google Scholar
  65. Gaume L, Forterre Y (2007) A viscoelastic deadly fluid in carnivorous pitcher plants. PLoS One 2:e1185PubMedPubMedCentralCrossRefGoogle Scholar
  66. Gaume L, Perret P, Gorb E, Gorb S, Labat JJ, Rowe N (2004) How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthropod Struct Dev 33:103–111PubMedCrossRefGoogle Scholar
  67. Givnish TJ (2015) New evidence on the origin of carnivorous plants. Proc Natl Acad Sci USA 112:10–11PubMedCrossRefGoogle Scholar
  68. Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromeliad Brocchinia reducta with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient poor habitats. Am Nat 124:479–497CrossRefGoogle Scholar
  69. González-Meler MA, Matamala R, Peñuelas J (1997) Effects of prolonged drought stress and nitrogen deficiency on the respiratory O2 uptake of bean and pepper leaves. Photosynthetica 34:505–512CrossRefGoogle Scholar
  70. Gorb E, Kastner V, Peressadko A, Arzt E, Gaume L, Rowe N, Gorb S (2004) Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention. J Exp Biol 207:2947–2963PubMedCrossRefGoogle Scholar
  71. Gratani L, Ghia E (2002) Adaptive strategy at the leaf level of Arbutus unedo L. to cope with Mediterranean climate. Flora 197:275–284CrossRefGoogle Scholar
  72. Grzesiak MT, Szczyrek P, Rut G, Ostrowska A, Hura K, Rzepka A, Hura T, Grzesiak S (2015) Interspecific differences in tolerance to soil compaction, drought and waterlogging stresses among maize and triticale genotypes. J Agro Crop Sci 201:330–343CrossRefGoogle Scholar
  73. Hájek T, Adamec L (2010) Photosynthesis and dark respiration of leaves of terrestrial carnivorous plants. Biologia 65:69–74CrossRefGoogle Scholar
  74. Halsted M, Lynch J (1996) Phosphorus responses of C3 and C4 species. J Exp Bot 47:497–505CrossRefGoogle Scholar
  75. Hamza MA, Anderson WK (2005) Soil compaction in cropping systems. Soil Till Res 82:121–145CrossRefGoogle Scholar
  76. Hao YS, Lei J, Wu XW, Wu LS, Jiang CC (2016) Photosynthate transport rather than photosynthesis rate is critical for low potassium adaptation of two cotton genotypes. Acta Agric Scand B-S P 66:170–177Google Scholar
  77. Haupt-Herting S, Klug K, Fock H (2001) A new approach to measure gross CO2 fluxes in leaves. Gross CO2 assimilation, photorespiration, and mitochondrial respiration in the light in tomato under drought stress. Plant Physiol 126:388–396PubMedPubMedCentralCrossRefGoogle Scholar
  78. He J, Zain A (2012) Photosynthesis and nitrogen metabolism of Nepenthes alata in response to inorganic NO3 and organic prey N in the greenhouse International Scholarly Research Network Botany ID 2e63270Google Scholar
  79. Hecht-Buchholz C (1967) Über die Dunkelfärbung des Blattgrüns bei Phosphormangel. Z Pflanzenernähr Bodenk 118:12–22CrossRefGoogle Scholar
  80. Henriques FS (1989) Effects of copper deficiency on the photosynthetic apparatus of sugar beet (Beta vulgaris L.). J Plant Physiol 135:453–458CrossRefGoogle Scholar
  81. Henriques FS (2001) Loss of blade photosynthetic area and of chloroplasts’ photochemical capacity account for reduced CO2 assimilation rates in zinc-deficient sugar beet leaves. J Plant Physiol 158:915–919CrossRefGoogle Scholar
  82. Henriques FS (2003) Gas exchange, chlorophyll a fluorescence kinetics and lipid peroxidation of pecan leaves with varying manganese concentrations. Plant Sci 165:239–244CrossRefGoogle Scholar
  83. Hepworth C, Doheny-Adams T, Hunt L, Cameron DD, Gray JE (2015) Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake. New Phytol 208:336–341PubMedPubMedCentralCrossRefGoogle Scholar
  84. Herold A (1980) Regulation of photosynthesis by sink activity – the missing link. New Phytol 86:131–144CrossRefGoogle Scholar
  85. Hikosaka K, Hanba YT, Hirose T, Terashima I (1998) Photosynthetic nitrogen-use efficiency in leaves of woody and herbaceous species. Funct Ecol 12:896–905CrossRefGoogle Scholar
  86. Hochmal AK, Schulze S, Trompelt K, Hippler M (2015) Calcium-dependent regulation of photosynthesis. Biochim Biophys Acta 1847:993–1003PubMedCrossRefGoogle Scholar
  87. Hu W, Yang J, Meng Y, Wang Y, Chen B, Zhao W, Oosterhuis DM, Zhou Z (2015) Potassium application affects carbohydrate metabolism in the leaf subtending the cotton (Gossypium hirsutum L.) boll and its relationship with boll biomass. Field Crop Res 179:120–131CrossRefGoogle Scholar
  88. Husted S, Laursen KH, Hebbern CA, Schmidt SB, Pedas P, Haldrup A, Jensen PE (2009) Manganese deficiency leads to genotype-specific changes in fluorescence induction kinetics and state transitions. Plant Physiol 150:825–833PubMedPubMedCentralCrossRefGoogle Scholar
  89. Ibrahim L, Proe MF, Cameron AD (1998) Interactive effects of nitrogen and water availabilities on gas exchange and whole plant carbon allocation in poplar. Tree Physiol 18:481–487PubMedCrossRefGoogle Scholar
  90. Jin J, Lauricella D, Armstrong R, Sale P, Tang C (2015) Phosphorus application and elevated CO2 enhance drought tolerance in field pea grown in a phosphorus-deficient vertisol. Ann Bot 116:975–985PubMedCrossRefPubMedCentralGoogle Scholar
  91. Kamaluddin M, Chang SX, Curran MP, Zwiazek JJ (2005) Soil compaction and forest floor removal affect early growth and physiology of lodgepole pine and Douglas-fir in British Columbia. For Sci 51:513–521Google Scholar
  92. Kanai S, Ohkura K, Adu-Gyamfi JJ, Mohapatra PK, Nguyen NT, Saneoka H, Fujita K (2007) Depression of sink activity precedes the inhibition of biomass production in tomato plants subjected to potassium deficiency stress. J Exp Bot 58:2917–2928PubMedCrossRefPubMedCentralGoogle Scholar
  93. Kao W-Y, Tsai T-T (1998) Tropic leaf movements, photosynthetic gas exchange, leaf ∆13C and chlorophyll a fluorescence of three soybean species in response to water availability. Plant Cell Environ 21:1055–1062CrossRefGoogle Scholar
  94. Karagatzides JD, Ellison AM (2009) Construction costs, payback times, and the leaf economics of carnivorous plants. Am J Bot 96:1612–1619PubMedCrossRefGoogle Scholar
  95. Kebbas S, Lutts S, Aid F (2015) Effect of drought stress on the photosynthesis of Acacia tortilis subsp. raddiana at the young seedling stage. Photosynthetica 53:288–298CrossRefGoogle Scholar
  96. Knight SE (1992) Costs of carnivory in the common bladderwort, Utricularia macrorhiza. Oecologia 89:348–355PubMedCrossRefGoogle Scholar
  97. Kobayashi T, Hori Y (2000) Photosynthesis and water-relation traits of the summer annual C4 grasses, Eleusine indica and Digitaria adscendens, with contrasting trampling tolerance. Ecol Res 15:165–174CrossRefGoogle Scholar
  98. Kobayashi T, Okamoto K, Hori Y (1999) Differences in field gas exchange and water relations between a C3 dicot (Plantago asiatica) and a C4 monocot, Eleusine indica. Photosynthetica 37:123–130CrossRefGoogle Scholar
  99. Kozlowski TT (1999) Soil compaction and growth of woody plants. Scand J For Res 14:596–619CrossRefGoogle Scholar
  100. Krapp A, Stitt M (1995) An evaluation of direct and indirect mechanisms for the sink regulation of photosynthesis in spinach - Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 195:313–323CrossRefGoogle Scholar
  101. Kriedemann PE, Anderson JE (1988) Growth and photosynthetic responses to manganese and copper deficiencies in wheat (Triticum aestivum) and barley grass (Hordeum glaucum and H. leporinum). Aust J Plant Physiol 15:429–446CrossRefGoogle Scholar
  102. Kriedemann PE, Graham RD, Wiskich JT (1985) Photosynthetic dysfunction and in vivo changes in chlorophyll a fluorescence from manganese-deficient wheat leaves. Aust J Agric Res 36:157–169CrossRefGoogle Scholar
  103. Kruse J, Gao P, Honsel A, Kreuzwiesser J, Burzlaff T, Alfarraj S, Hedrich R, Rennenberg H (2014) Strategy of nitrogen acquisition and utilization by carnivorous Dionaea muscipula. Oecologia 174:839–851PubMedCrossRefGoogle Scholar
  104. Kumar P, Kumar Tewari R, Sharma PN (2008) Modulation of copper toxicity-induced oxidative damage by excess supply of iron in maize plants. Plant Cell Rep 27:399–409PubMedCrossRefGoogle Scholar
  105. Kutschera U, Briggs WR (2016) Phototropic solar tracking in sunflower plants: an integrative perspective. Ann Bot 117(1):1–8PubMedPubMedCentralCrossRefGoogle Scholar
  106. Kyparissis A, Drilias P, Manetas Y (2000) Seasonal fluctuations in photoprotective (xanthophyll cycle) and photoselective (chlorophylls) capacity in eight Mediterranean plant species belonging to two different growth forms. Aust J Plant Physiol 27:265–272Google Scholar
  107. Larbi A, Morales F, Abadía A, Gogorcena Y, Lucena JJ, Abadía J (2002) Effects of Cd and Pb in sugar beet plants grown in nutrient solution: induced Fe deficiency and growth inhibition. Funct Plant Biol 29:1453–1464CrossRefGoogle Scholar
  108. 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 89:113–126PubMedCrossRefGoogle Scholar
  109. Lauer MJ, Pallardy SG, Blevins DG, Randall DD (1989) Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.). Plant Physiol 91:848–854PubMedPubMedCentralCrossRefGoogle Scholar
  110. Lawlor DW (1995) The effects of water deficit on photosynthesis. In: Smirnoff M (ed) Environment and plant metabolism. Flexibility and acclimation. BIOS Scientific, Oxford, pp 129–160Google Scholar
  111. Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol 97:1–13CrossRefGoogle Scholar
  112. 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. J Exp Bot 6:2351–2360CrossRefGoogle Scholar
  113. Li Z, Wu N, Liu T, Chen H, Tang M (2015) Effect of arbuscular mycorrhizal inoculation on water status and photosynthesis of Populus cathayana males and females under water stress. Physiol Plant 155:192–204PubMedCrossRefPubMedCentralGoogle Scholar
  114. Liu XY, Cui HQ, Li AN, Zhang M, Teng YB (2015a) The nitrate transporter NRT1.1 is involved in iron deficiency responses in Arabidopsis. J Plant Nutr Soil Sci 178:601–608CrossRefGoogle Scholar
  115. Liu CX, Rubaek GH, Liu FL, Andersen MN (2015b) Effect of partial root zone drying and deficit irrigation on nitrogen and phosphorus uptake in potato. Agric Water Manage 159:66–76CrossRefGoogle Scholar
  116. Loeppert RH (1986) Reactions of iron and carbonates in calcareous soils. J Plant Nutr 9:195–215CrossRefGoogle Scholar
  117. Logan BA, Demmig-Adams B, Rosenstiel TN, Adams WW III (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209:213–220PubMedCrossRefPubMedCentralGoogle Scholar
  118. Lokhande SB, Reddy KR (2015) Cotton reproductive and fiber quality responses to nitrogen nutrition. Int J Plant Prod 9:191–210Google Scholar
  119. Lösch R, Jensen CR, Andersen MN (1992) Diurnal courses and factorial dependencies of leaf conductance and transpiration of differently potassium fertilized and watered field grown barley plants. Plant Soil 140:205–224CrossRefGoogle Scholar
  120. Macrobbie EAC (1998) Signal transduction and ion channels in guard cells. Philos T Roy Soc B 353:1475–1488CrossRefGoogle Scholar
  121. Makino A, Osmond CB (1991) Effects of nitrogen nutrition on nitrogen partitioning between chloroplast and mitochondria in pea and wheat. Plant Physiol 96:355–362PubMedPubMedCentralCrossRefGoogle Scholar
  122. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  123. Marschner H, Cakmak I (1989) High light intensity enhances chlorosis and necrosis in leaves of zinc-, potassium- and magnesium-deficient bean (Phaseolus vulgaris) plants. J Plant Physiol 134:308–315CrossRefGoogle Scholar
  124. Mattiello EM, Ruiz HA, Neves JCL, Ventrella MC, Araujo WL (2015) Zinc deficiency affects physiological and anatomical characteristics in maize leaves. J Plant Physiol 183:138–143PubMedCrossRefGoogle Scholar
  125. Medrano H, Parry MAJ, Socías X, Lawlor DW (1998) Long term water stress inactivates Rubisco in subterranean clover. Ann Appl Biol 131:491–501CrossRefGoogle Scholar
  126. Medrano H, Bota J, Abadía A, Sampól B, Escalona JM, Flexas J (2002) Effects of drought on light-energy dissipation mechanisms in high-light-acclimated, field-grown grapevines. Funct Plant Biol 29:1197–1207CrossRefGoogle Scholar
  127. Méndez M, Karlsson PS (1999) Costs and benefits of carnivory in plants: insights from the photosynthetic performance of four carnivorous plants in a subarctic environment. Oikos 86:105–112CrossRefGoogle Scholar
  128. Michalko J, Socha P, Mészáros P, Blehová A, Libantová J, Moravčíková J, Matušíková I (2013) Glucan-rich diet is digested and taken up by the carnivorous sundew (Drosera rotundifolia L.): implication for a novel role of plant β-1,3-glucanases. Planta 238:715–725PubMedCrossRefGoogle Scholar
  129. Mofokeng MM, Steyn JM, du Plooy CP, Prinsloo G, Araya HT (2015) Growth of Pelargonium sidoides DC. in response to water and nitrogen level. S Afr J Bot 100:183–189CrossRefGoogle Scholar
  130. Morales F, Warren CR (2012) Photosynthetic responses to nutrient deprivation and toxicities. In: Flexas J, Loreto F, Medrano H (eds) Terrestrial photosynthesis in a changing environment: a molecular, physiological and ecological approach. Cambridge University Press, Cambridge, pp 312–330CrossRefGoogle Scholar
  131. Morales F, Abadía A, Abadía J (1990) Characterization of the xanthophyll cycle and other photosynthetic pigment changes induced by iron deficiency in sugar beet (Beta vulgaris L.). Plant Physiol 94:607–613PubMedPubMedCentralCrossRefGoogle Scholar
  132. Morales F, Abadía A, Abadía J (1991) Chlorophyll fluorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. Plant Physiol 97:886–893PubMedPubMedCentralCrossRefGoogle Scholar
  133. Morales F, Belkhodja R, Abadía A, Abadía J (1994) Iron deficiency-induced changes in the photosynthetic pigment composition of field-grown pear (Pyrus communis L.) leaves. Plant Cell Environ 17:1153–1160CrossRefGoogle Scholar
  134. Morales F, Abadía A, Abadía J (1998) Photosynthesis, quenching of chlorophyll fluorescence and thermal energy dissipation in iron-deficient sugar beet leaves. Aust J Plant Physiol 25:403–412CrossRefGoogle Scholar
  135. Morales F, Abadía A, Abadía J (2006) Photoinhibition and photoprotection under nutrient deficiencies, drought and salinity. In: Demmig-Adams B, Adams IIIWW, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. Springer, Dordrecht, pp 65–85CrossRefGoogle Scholar
  136. Muneer S, Jeong BR (2015) Silicon decreases Fe deficiency responses by improving photosynthesis and maintaining composition of thylakoid multiprotein complex proteins in soybean plants (Glycine max L.). J Plant Growth Regul 34:485–498CrossRefGoogle Scholar
  137. Munné-Bosch S, Alegre L (2000) The significance of ß-carotene, α-tocopherol and the xanthophyll cycle in droughted Melissa officinalis plants. Aust J Plant Physiol 27:139–146Google Scholar
  138. Murad E, Fisher WR (1988) Iron in soils and clay minerals. D Reidel Publishing Co, DordrechtGoogle Scholar
  139. Neals TF, Incoll LD (1968) The control of leaf photosynthesis rate by the level of assimilate concentration in the leaf: a review of hypotheses. Bot Rev 34:107–125CrossRefGoogle Scholar
  140. Nishio JN (2000) Why are higher plants green? Evolution of the higher plant photosynthetic pigment complement. Plant Cell Environ 23:539–448CrossRefGoogle Scholar
  141. Ogren WL, Bowes G (1971) Ribulose diphosphate carboxylase regulates soybean photorespiration. Nature 230:159–160Google Scholar
  142. Ohki K (1976) Effect of zinc nutrition on photosynthesis and carbonic anhydrase activity in cotton. Physiol Plant 38:300–304CrossRefGoogle Scholar
  143. Ohki K (1985) Manganese deficiency and toxicity effects on photosynthesis, chlorophyll, and transpiration in wheat. Crop Sci 25:187–191CrossRefGoogle Scholar
  144. Ohki K, Wilson DO, Anderson OE (1981) Manganese deficiency and toxicity sensitivities of soybean cultivar. Agron J 72:713–716CrossRefGoogle Scholar
  145. Osunkoya OO, Daud SD, Di-Giusto B, Wimmer FL, Holige TM (2007) Construction costs and physico-chemical properties of the assimilatory organs of Nepenthes species in northern Borneo. Ann Bot 99:895–906PubMedPubMedCentralCrossRefGoogle Scholar
  146. Ouzounidou G, Ilias I, Tranopoulou H, Karataglis S (1998) Amelioration of copper toxicity by iron on spinach physiology. J Plant Nutr 21:2089–2101CrossRefGoogle Scholar
  147. Paul MJ, Driscoll SP (1997) Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance. Plant Cell Environ 20:110–116CrossRefGoogle Scholar
  148. Pavlovič A (2011) Photosynthetic characterization of Australian pitcher plant Cephalotus follicularis. Photosynthetica 49:253–258CrossRefGoogle Scholar
  149. Pavlovič A, Saganová L (2015) A novel insight into the cost–benefit model for the evolution of botanical carnivory. Ann Bot 115:1075–1092PubMedPubMedCentralCrossRefGoogle Scholar
  150. Pavlovič A, Masarovičová E, Hudák J (2007) Carnivorous syndrome in Asian pitcher plants of the genus Nepenthes. Ann Bot 100:527–536PubMedPubMedCentralCrossRefGoogle Scholar
  151. Pavlovič A, Singerová L, Demko V, Hudák J (2009) Feeding enhances photosynthetic efficiency in the carnivorous pitcher plant Nepenthes talangensis. Ann Bot 104:307–314PubMedPubMedCentralCrossRefGoogle Scholar
  152. Pavlovič A, Demko V, Hudák J (2010a) Trap closure and prey retention in Venus flytrap (Dionaea muscipula Ellis.) temporarily reduces photosynthesis and stimulates respiration. Ann Bot 105:37–44PubMedCrossRefGoogle Scholar
  153. Pavlovič A, Singerová L, Demko V, Šantrůček J, Hudák J (2010b) Root nutrient uptake enhances photosynthetic assimilation in prey-deprived carnivorous pitcher plant Nepenthes talangensis. Photosynthetica 48:227–233CrossRefGoogle Scholar
  154. Pavlovič A, Slováková Ľ, Pandolfi C, Mancuso S (2011a) On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis.). J Exp Bot 62:1991–2000PubMedPubMedCentralCrossRefGoogle Scholar
  155. Pavlovič A, Slováková Ľ, Šantrůček J (2011b) Nutritional benefit from leaf litter utilization in the pitcher plants Nepenthes ampullaria. Plant Cell Environ 34:1865–1873PubMedCrossRefGoogle Scholar
  156. Pavlovič A, Krausko M, Libiaková M, Adamec L (2014) Feeding on prey increases photosynthetic efficiency in the carnivorous sundew Drosera capensis. Ann Bot 113:69–78PubMedCrossRefGoogle Scholar
  157. Pavlovič A, Krausko M, Adamec L (2016) A carnivorous sundew plant prefers protein over chitin as a source of nitrogen from its traps. Plant Physiol Biochem 104:11–16PubMedCrossRefGoogle Scholar
  158. Pieters AJ, Paul MJ, Lawlor DW (2001) Low sink demand limits photosynthesis under Pi deficiency. J Exp Bot 52:1083–1091PubMedCrossRefGoogle Scholar
  159. Plesnicar M, Kastori R, Petrovic N, Pankovic D (1994) Photosynthesis and chlorophyll fluorescence in sunflower (Helianthus annuus L.) leaves as affected by phosphorus nutrition. J Exp Bot 45:919–924CrossRefGoogle Scholar
  160. Polanco MC, Zwiazek JJ, Voicu MC (2008) Responses of ectomycorrhizal American elm (Ulmus americana) seedlings to salinity and soil compaction. Plant Soil 308:189–200CrossRefGoogle Scholar
  161. Rao IM, Terry N (1989) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas exchange and Calvin cycle enzymes. Plant Physiol 90:814–819PubMedPubMedCentralCrossRefGoogle Scholar
  162. Rao IM, Terry N (1995) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. IV: changes with time following increased supply of phosphate to low phosphate plants. Plant Physiol 107:1313–1321PubMedPubMedCentralCrossRefGoogle Scholar
  163. Reich PB (1993) Reconciling apparent discrepancies among studies relating life-span, structure and function of leaves in contrasting plant life forms and climates – the blind men and the elephant retold. Funct Ecol 7:721–725CrossRefGoogle Scholar
  164. Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734PubMedCrossRefGoogle Scholar
  165. Reich PB, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Funct Ecol 12:948–958CrossRefGoogle Scholar
  166. Rischer H, Hamm A, Bringmann G (2002) Nepenthes insignis uses a C2-portion of the carbon skeleton of L-alanine acquired via its carnivorous organs, to build up the allelochemical plumbagin. Phytochemistry 59:603–609PubMedCrossRefGoogle Scholar
  167. Sage RF, Pearcy RW (1987a) The nitrogen use efficiency of C3 and C4 plants. I. Leaf nitrogen, growth and biomass partitioning in Chenopodium album L. and Amaranthus retroflexus L. Plant Physiol 84:954–958PubMedPubMedCentralCrossRefGoogle Scholar
  168. Sage RF, Pearcy RW (1987b) The nitrogen use efficiency of C3 and C4 plants. II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album L. and Amaranthus retroflexus L. Plant Physiol 84:959–963PubMedPubMedCentralCrossRefGoogle Scholar
  169. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (2006) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low phosphorus-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiol 140:879–889PubMedPubMedCentralCrossRefGoogle Scholar
  170. Sanhueza C, Bascunan-Godoy L, Turnbull MH, Corcuera LJ (2015) Response of photosynthesis and respiration to temperature under water deficit in two evergreen Nothofagus species. Plant Spec Biol 30:163–175CrossRefGoogle Scholar
  171. Sawada S, Usuda H, Tsukui T (1992) Participation of inorganic orthophosphate in regulation of the Ribulose-1,5-bisphosphate carboxylase activity in response to changes in the photosynthetic source-sink balance. Plant Cell Physiol 33:943–949Google Scholar
  172. Schroeder JI (2003) Knockout of the guard cell K+ out channel and stomatal movements. Proc Natl Acad Sci USA 100:4976–4977PubMedCrossRefGoogle Scholar
  173. Schuerger AC, Capelle GA, Di Benedetto JA, Mao C, Thai CN, Evans MD, Richards JT, Blank TA, Stryjewski EC (2003) Comparison of two hyperspectral imaging and two laser-induced fluorescence instruments for the detection of zinc stress and chlorophyll concentration in bahia grass (Paspalum notatum Flugge.). Remote Sens Environ 84:572–588CrossRefGoogle Scholar
  174. Shahbaz M, Ravet K, Peers G, Pilon M (2015) Prioritization of copper for the use in photosynthetic electron transport in developing leaves of hybrid poplar. Front Plant Sci 6:407PubMedPubMedCentralCrossRefGoogle Scholar
  175. Sharma PN, Tripathi A, Bisht SS (1995) Zinc requirement for stomatal opening in cauliflower. Plant Physiol 107:751–756PubMedPubMedCentralCrossRefGoogle Scholar
  176. Sheriff DW, Nambiar EKS (1991) Nitrogen nutrition, growth and gas exchange in Eucalyptus globulus Labill seedlings. Aust J Plant Physiol 18:37–52CrossRefGoogle Scholar
  177. Silva EN, Ribeiro RV, Ferreira-Silva SL, Vieira SA, Ponte LFA, Silveira JAG (2012) Coordinate changes in photosynthesis, sugar accumulation and antioxidant enzymes improve the performance of Jatropha curcas plants under drought stress. Biomass Bioenerg 45:270–279CrossRefGoogle Scholar
  178. 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
  179. 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 Biol 151:276–284CrossRefGoogle Scholar
  180. Snider JL, Chastain DR, Meeks CD, Collins GD, Sorensen RB, Byrd SA, Perry CD (2015) Predawn respiration rates during flowering are highly predictive of yield response in Gossypium hirsutum when yield variability is water-induced. J Plant Physiol 183:114–120PubMedCrossRefGoogle Scholar
  181. Solti A, Gáspár L, Mészáros I, Szigeti Z, Lévai L, Sárvári E (2008) Impact of iron supply on the kinetics of recovery of photosynthesis in Cd-stressed poplar (Populus glauca). Ann Bot 102:771–782PubMedPubMedCentralCrossRefGoogle Scholar
  182. Souza RP, Machado EC, Silva JAB, Lagoa AMMA, Silveira JAG (2004) Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ Exp Bot 51:45–56CrossRefGoogle Scholar
  183. Sun J, Nishio JN, Vogelmann TC (1996a) 35S-Methionine incorporates differentially into polypeptides across leaves of spinach (Spinacia oleracea). Plant Cell Physiol 37:996–1006CrossRefGoogle Scholar
  184. Sun J, Nishio JN, Vogelmann TC (1996b) High-light effects on CO2 fixation gradients across leaves. Plant Cell Environ 19:1261–1271CrossRefGoogle Scholar
  185. Takizawa K, Kanazawa A, Kramer DM (2008) Depletion of stromal Pi induces high ‘energy-dependent’ antenna exciton quenching (q(E)) by decreasing proton conductivity at CFO-CF1 ATP synthase. Plant Cell Environ 31:235–243PubMedPubMedCentralCrossRefGoogle Scholar
  186. Taylor SE, Terry N (1986) Variation in photosynthetic electron transport capacity and its effect on the light modulation of ribulose bisphosphate carboxylase. Photosynth Res 8:249–256PubMedCrossRefPubMedCentralGoogle Scholar
  187. Terashima I, Evans JR (1988) Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant Cell Physiol 29:143–155Google Scholar
  188. Terry N, Abadía J (1986) Function of iron in chloroplasts. J Plant Nutr 9:609–646CrossRefGoogle Scholar
  189. Terry N, Ulrich A (1973a) Effects of potassium deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 51:783–786PubMedPubMedCentralCrossRefGoogle Scholar
  190. Terry N, Ulrich A (1973b) Effects of phosphorus deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 51:43–47PubMedPubMedCentralCrossRefGoogle Scholar
  191. Terry N, Ulrich A (1974) Photosynthetic and respiratory CO2 exchange of sugar beet as influenced by manganese deficiency. Crop Sci 14:502–504CrossRefGoogle Scholar
  192. Thorén LM, Tuomi J, Kämäräinen T, Laine K (2003) Resource availability affects investment in carnivory in Drosera rotundifolia. New Phytol 159:507–511CrossRefGoogle Scholar
  193. Timperio AM, D’Amici GM, Barta C, Loreto F, Zolla L (2007) Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J Exp Bot 58:3695–3710PubMedCrossRefPubMedCentralGoogle Scholar
  194. Toenniessen GH (1984) Review of the world food situation and the role of salt-tolerant plants. In: Staples RC, Toenniessen GH (eds) Salinity tolerance of plants. Wiley-Interscience, New York, pp 399–413Google Scholar
  195. Tubeileh A, Groleau-Renaud V, Plantureux S, Guckert A (2003) Effect of soil compaction on photosynthesis and carbon partitioning within a maize-soil system. Soil Till Res 71:151–161CrossRefGoogle Scholar
  196. Turnbull TL, Warren CR, Adams MA (2007) Novel mannose-sequestration technique reveals variation in subcellular orthophosphate pools do not explain the effects of phosphorus nutrition on photosynthesis in Eucalyptus globulus seedlings. New Phytol 176:849–861PubMedCrossRefPubMedCentralGoogle Scholar
  197. Urban L, Jegouzo L, Damour G, Vandame M, François C (2008) Interpreting the decrease in leaf photosynthesis during flowering in mango. Tree Physiol 28:1025–1036PubMedCrossRefGoogle Scholar
  198. 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 (Quercus cerris L.) leaves: diurnal cycles under different levels of water supply. Plant Cell Environ 18:631–640CrossRefGoogle Scholar
  199. van Assche FV, Clijsters H (1986) Inhibition of photosynthesis by treatment of Phaseolus vulgaris with toxic concentration of zinc: effects on electron transport and photophosphorylation. Physiol Plant 66:717–721CrossRefGoogle Scholar
  200. Van den Akker JJH, Canarache A (2001) Two European concerted actions on subsoil compaction. Land Use and Development 42:15–22Google Scholar
  201. van der Ent A, Sumail S, Clarke C (2015) Habitat differentiation of obligate ultramafic Nepenthes endemic to Mount Kinabalu and Mount Tambuyukon (Sabah, Malaysia). Plant Ecol 216:789–807CrossRefGoogle Scholar
  202. Vincent O, Roditchev I, Marmottant P (2011a) Spontaneous firings of carnivorous aquatic Utricularia traps: Temporal patterns and mechanical oscillations. PLoS One 6:e20205PubMedPubMedCentralCrossRefGoogle Scholar
  203. Vincent O, Weißkopf C, Poppinga S, Masselter T, Speck T, Joyeux M, Quilliet C, Marmottant P (2011b) Ultra-fast underwater suction traps. P R Soc B Biol Sci 278:2909–2914CrossRefGoogle Scholar
  204. Volkov AG, Adesina T, Markin VS, Jovanov E (2008) Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol 146:694–702PubMedPubMedCentralCrossRefGoogle Scholar
  205. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387CrossRefGoogle Scholar
  206. Walcroft AS, Whitehead D, Silvester WB, Kelliher FM (1997) The response of photosynthetic model parameters to temperature and nitrogen concentration in Pinus radiata D. Don. Plant Cell Environ 20:1338–1348CrossRefGoogle Scholar
  207. Walker DA, Sivak MN (1985) Can phosphate limit photosynthetic carbon assimilation in vivo? Physiol Veg 23:829–841Google Scholar
  208. Walker DA, Sivak MN (1986) Photosynthesis and phosphate: a cellular affair? Trends Biochem Sci 11:176–179CrossRefGoogle Scholar
  209. Wang H, Jin JY (2005) Photosynthetic rate, chlorophyll fluorescence parameters, and lipid peroxidation of maize leaves as affected by zinc deficiency. Photosynthetica 43:591–596CrossRefGoogle Scholar
  210. Wang X, Shi Y, Guo ZJ, Zhang YL, Yu ZW (2015a) Water use and soil nitrate nitrogen changes under supplemental irrigation with nitrogen application rate in wheat field. Field Crop Res 183:117–125CrossRefGoogle Scholar
  211. Wang X-G, Zhao X-H, Jiang C-J, Li C-H, Cong S, Wu D, Chen Y-Q, Yu H-Q, Wang C-Y (2015b) Effects of potassium deficiency on photosynthesis and photoprotection mechanisms in soybean (Glycine max (L.) Merr.). J Integr Agric 14:856–863CrossRefGoogle Scholar
  212. Warren CR (2004) The photosynthetic limitation posed by internal conductance to CO2 movement is increased by nutrient supply. J Exp Bot 55:2313–2321PubMedCrossRefGoogle Scholar
  213. Warren CR, Adams MA (2002) Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster. Tree Physiol 22:11–19PubMedCrossRefGoogle Scholar
  214. Weng XY, Zheng CJ, Xu HX, Sun JY (2007) Characteristics of photosynthesis and functions of the water-water cycle in rice (Oryza sativa) leaves in response to potassium deficiency. Physiol Plant 131:614–621PubMedCrossRefGoogle Scholar
  215. Weng XY, Xu HX, Yang Y, Peng HH (2008) Water-water cycle involved in dissipation of excess photon energy in phosphorus deficient rice leaves. Biol Plant 52:307–313CrossRefGoogle Scholar
  216. Winder TL, Nishio J (1995) Early iron deficiency stress response in leaves of sugar beet. Plant Physiol 108:1487–1494PubMedPubMedCentralCrossRefGoogle Scholar
  217. Wolfe DW, Topoleski DT, Gundersheim NA, Ingall BA (1995) Growth and yield sensitivity of 4 vegetable crops to soil compaction. J Am Soc Hortic Sci 120:956–963Google Scholar
  218. Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants-a retrospective analysis of the A/Ci curves from 109 species. J Exp Bot 44:907–920CrossRefGoogle Scholar
  219. Xu HX, Weng XY, Yang Y (2007) Effect of phosphorus deficiency on the photosynthetic characteristics of rice plants. Russ J Plant Physiol 54:741–748CrossRefGoogle Scholar
  220. Xu CP, Jiang ZC, Huang BR (2011) Nitrogen deficiency-induced protein changes in immature and mature leaves of creeping bentgrass. J Am Soc Hortic Sci 136:399–407Google Scholar
  221. Yan N, Zhang YL, Xue HM, Zhang XH, Wang ZD, Shi LY, Guo DP (2015) Changes in plant growth and photosynthetic performance of Zizania latifolia exposed to different phosphorus concentrations under hydroponic condition. Photosynthetica 53:630–635CrossRefGoogle Scholar
  222. Yin X, Struik PC, Romero P, Harbinson J, Evers JB, Van der Putten PEL, Vos J (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 32:448–464PubMedCrossRefGoogle Scholar
  223. Yu Q, Osborne L, Rengel Z (1998) Micronutrient deficiency changes activities of superoxide dismutase and ascorbate peroxidase in tobacco plants. J Plant Nutr 21:1427–1437CrossRefGoogle Scholar
  224. Zamora R, Gómez JM, Hódar JA (1998) Fitness responses of a carnivorous plant in contrasting ecological scenarios. Ecology 79:1630–1644CrossRefGoogle Scholar
  225. Zargar SM, Agrawal GK, Rakwal R, Fukao Y (2015) Quantitative proteomics reveals role of sugar in decreasing photosynthetic activity due to Fe deficiency. Front Plant Sci 6:592PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Fermín Morales
    • 1
    • 2
    Email author
  • Andrej Pavlovič
    • 3
  • Anunciación Abadía
    • 1
  • Javier Abadía
    • 1
  1. 1.Department of Plant Nutrition, Experimental Station of Aula Dei-EEADConsejo Superior de Investigaciones Científicas-CSICApdo, ZaragozaSpain
  2. 2.Instituto de Agrobiotecnología (IdAB)Universidad Pública de Navarra-CSIC-Gobierno de NavarraNavarraSpain
  3. 3.Department of Biophysics, Centre of the Region Haná for Biotechnological and Agricultural ResearchPalacký UniversityOlomoucCzech Republic

Personalised recommendations