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Light quality affects light harvesting and carbon sequestration during the diel cycle of crassulacean acid metabolism in Phalaenopsis

  • Liang Zheng
  • Johan Ceusters
  • Marie-Christine Van LabekeEmail author
Original Article

Abstract

Crassulacean acid metabolism (CAM) is a specialized photosynthetic pathway present in a variety of genera including many epiphytic orchids. CAM is under circadian control and can be subdivided into four discrete phases during a diel cycle. Inherent to this specific mode of metabolism, carbohydrate availability is a limiting factor for nocturnal CO2 uptake and biomass production. To evaluate the effects of light quality on the photosynthetic performance and diel changes in carbohydrates during the CAM cycle. Phalaenopsis plants were grown under four different light qualities (red, blue, red + blue and full spectrum white light) at a fluence of 100 µmol m−2 s−1 and a photoperiod of 12 h for 8 weeks. In contrast to monochromatic blue light, plants grown under monochromatic red light showed already a significant decline of the quantum efficiency (ΦPSII) after 5 days and of the maximum quantum yield (Fv/Fm) after 10 days under this treatment. This was also reflected in a compromised chlorophyll and carotenoid content and total diel CO2 uptake under red light in comparison with monochromatic blue and full spectrum white light. In particular, CO2 uptake during nocturnal phase I was affected under red illumination resulting in a reduced amount of vacuolar malate. In addition, red light caused the rate of decarboxylation of malate during the day to be consistently lower and malic acid breakdown persisted until 4 h after dusk. Because the intrinsic activity of PEPC was not affected, the restricted availability of storage carbohydrates such as starch was likely to cause these adverse effects under red light. Addition of blue to the red light spectrum restored the diel fluxes of carbohydrates and malate and resulted in a significant enhancement of the daily CO2 uptake, pigment concentration and biomass formation.

Keywords

CAM Phalaenopsis Carbohydrates Gas exchange PEPC Malate 

Notes

Acknowledgements

The first author received a CSC scholarship and a funding from Ghent University (BOF14/CHN/012).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abraham PE, Yin H, Borland AM, Weighill D, Lim SD, De Paoli HC, Engle N, Jones PC, Agh R, Weston DJ, Wullschleger SD, Tschaplinski T, Jacobson D, Cushman JC, Hettich RL, Tuskan GA, Yang X (2016) Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. Nat Plants 2:16178.  https://doi.org/10.1038/nplants.2016.178 Google Scholar
  2. Adams WW, Díaz M, Winter K (1989) Diurnal changes in photochemical efficiency, the reduction state of Q, radiationless energy dissipation, and non-photochemical fluorescence quenching in cacti exposed to natural sunlight in northern Venezuela. Oecologia 80:553–561.  https://doi.org/10.1007/BF00380081 Google Scholar
  3. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113.  https://doi.org/10.1146/annurev.arplant.59.032607.092759 Google Scholar
  4. Barrow SR, Cockburn W (1982) Effects of light quantity and quality on the decarboxylation of malic Acid in crassulacean Acid metabolism photosynthesis. Plant Physiol 69(3):568–571Google Scholar
  5. Boccalandro E, Giordano CV, Ploschuk EL, Piccoli PN (2012) Phototropins but not cryptochromes mediate the blue light-specific promotion of stomatal conductance, while both enhance photosynthesis and transpiration under. Plant Physiol 158:1475–1484.  https://doi.org/10.1104/pp.111.187237 Google Scholar
  6. Borland AM, Dodd AN (2002) Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest. Funct Plant Biol 29:707–716.  https://doi.org/10.1071/PP01221 Google Scholar
  7. Borland AM, Zambrano VAB, Ceusters J, Shorrock K (2011) The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytol 191(3):619–633.  https://doi.org/10.1111/j.1469-8137.2011.03781.x Google Scholar
  8. Brulfert J, Kluge M, Güçlü S, Queiroz O (1988) Interaction of photoperiod and drought as CAM inducing factors in Kalanchoë blossfeldiana Poelln., cv. Tom Thumb J Plant Physiol 133:222–227.  https://doi.org/10.1016/S0176-1617(88)80141-X Google Scholar
  9. Ceusters J, Borland AM, Londers E, Verdoodt V, Godts C, De Proft MP (2009) Differential usage of storage carbohydrates in the CAM bromeliad Aechmea ‘Maya’ during acclimation to drought and recovery from dehydration. Physiol Plant 135:174–184.  https://doi.org/10.1111/j.1399-3054.2008.01186.x Google Scholar
  10. Ceusters J, Borland AM, Ceusters N, Verdoodt V, Godts C, De Proft MP (2010a) Seasonal influences on carbohydrate metabolism in the CAM bromeliad Aechmea “Maya”: consequences for carbohydrate partitioning and growth. Ann Bot 105:301–309.  https://doi.org/10.1093/aob/mcp275 Google Scholar
  11. Ceusters J, Godts C, Proft MPD (2010b) Differential usage of storage carbohydrates in the cam bromeliad Aechmea ‘Maya’ during acclimation to drought and recovery from dehydration. Physiol Plant 135(2):174–184.  https://doi.org/10.1111/j.1399-3054.2008.01186.x Google Scholar
  12. Ceusters J, Borland AM, Godts C, Londers E, Croonenborghs S, Van Goethem D, De Proft MP (2011) Crassulacean acid metabolism under severe light limitation: a matter of plasticity in the shadows?Google Scholar
  13. Ceusters J, Borland AM, Taybi T, Frans M, Godts C, De Proft MP (2014) Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism. J Exp Bot 65:3705–3714.  https://doi.org/10.1093/jxb/eru185 Google Scholar
  14. Dietzel L, Bräutigam K, Pfannschmidt T (2008) Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry—functional relationships between short-term and long-term light quality acclimation in plants. FEBS J 275:1080–1088.  https://doi.org/10.1111/j.1742-4658.2008.06264.x Google Scholar
  15. Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K (2002) Crassulacean acid metabolism: plastic, fantastic. J Exp Bot 53:569–580.  https://doi.org/10.1093/jexbot/53.369.569 Google Scholar
  16. Fankhauser C, Chory J (1997) Light control of plant development. Annu Rev Cell Dev Biol 13:203–229.  https://doi.org/10.1146/annurev.cellbio.13.1.203 Google Scholar
  17. Ferroni L (2012) Photosynthetic acclimation to the light environment: molecular mechanisms to understand plant consortia. J Ecosyst Ecogr 2:1–2.  https://doi.org/10.4172/2157-7625.1000e104 Google Scholar
  18. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883.  https://doi.org/10.1042/BCJ20160814 Google Scholar
  19. Grams TEE, Thiel S (2002) High light-induced switch from C(3)-photosynthesis to Crassulacean acid metabolism is mediated by UV-A/blue light. J Exp Bot 53:1475–1483.  https://doi.org/10.1093/jexbot/53.373.1475 Google Scholar
  20. Griffiths H (1989) Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes. In: Lüttge U (ed) Vascular Plants as Epiphytes: Evolution and Ecophysiology. Springer, Berlin, pp 42–86.  https://doi.org/10.1007/978-3-642-74465-5_3 Google Scholar
  21. Guo W-J, Lee N (2006) Effect of leaf and plant age, and day/night temperature on net CO2 uptake in Phalaenopsis amabilis var. formosa. J Am Soc Hort Sci 131:320–326Google Scholar
  22. Hoffmann AM, Noga G, Hunsche M (2015) Acclimations to light quality on plant and leaf level affect the vulnerability of pepper (Capsicum annuum L.) to water deficit. J Plant Res 128:295–306.  https://doi.org/10.1007/s10265-014-0698-z Google Scholar
  23. Holtum JAM, Smith JAC, Neuhaus HE (2005) Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Funct Plant Biol 32:429–449Google Scholar
  24. Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99.  https://doi.org/10.1046/j.1365-3040.2001.00648.x Google Scholar
  25. Krause GH, Somersalo S, Zumbusch E, Weyers B, Laasch H (1990) On the mechanism of photoinhibition in chloroplasts. relationship between changes in fluorescence and activity of photosystem II. J Plant Physiol 136:472–479.  https://doi.org/10.1016/S0176-1617(11)80038-6 Google Scholar
  26. Lee JS (2010) Stomatal opening mechanism of CAM plants. J Plant Biol 53:19–23.  https://doi.org/10.1007/s12374-010-9097-8 Google Scholar
  27. Lee DM, Assmann SM (1992) Stomatal responses to light in the facultative Crassulacean acid metabolism species, Pottulacaria afra. Physiol Plant 85:35–42.  https://doi.org/10.1111/j.1399-3054.1992.tb05260.x Google Scholar
  28. Liscum E, Hodgson DW, Campbell TJ (2003) Update on blue light signaling blue light signaling through the cryptochromes and phototropins. So that’s what the blues is all about. Society 133:1429–1436.  https://doi.org/10.1104/pp.103.030601 Google Scholar
  29. López-Millán AF, Morales F, Andaluz S, Gogorcena Y, Abadía A, Rivas JD, Las JA, Lo AF, Gogorcena Y, Rivas JD, Las JA (2000) Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use 1. Plant Physiol 124:885–897Google Scholar
  30. Lüttge U (2002) CO2-concentrating: consequences in crassulacean acid metabolism. J Exp Bot 53(378):2131–2142.  https://doi.org/10.1093/jxb/erf081 Google Scholar
  31. Males J, Griffiths H (2017) Stomatal biology of CAM plants. Plant Physiol.  https://doi.org/10.1104/pp.17.00114 Google Scholar
  32. Mc Williams EL (1970) Comparative rates of dark CO2 uptake and acidification in the Bromeliaceae, Orchidaceae, and Euphorbiaceae. Bot Gaz 131:285–290.  https://doi.org/10.1086/336545 Google Scholar
  33. McCree KJ (1971) The action spectrum, absorptance and quantum yield of photosynthesis in crop plants. Agric Meteorol 9:191–216.  https://doi.org/10.1016/0002-1571(71)90022-7 Google Scholar
  34. Nelson EA, Sage RF (2008) Functional constraints of CAM leaf anatomy: tight cell packing is associated with increased CAM function across a gradient of CAM expression. J Exp Bot 59:1841–1850.  https://doi.org/10.1093/jxb/erm346 Google Scholar
  35. Nishida K, Hayashi Y (1981) Inhibition of deacidification by photosynthesis inhibitors in Kalanchoe pinnatum (= Bryophyllum calycinum). Plant Sci Lett 19:271–276Google Scholar
  36. Olle M, Viršile A (2013) The effects of light-emitting diode lighting on greenhouse plant growth and quality. Agric Food Sci 22:223–234.  https://doi.org/10.1016/j.envexpbot.2009.06.011 Google Scholar
  37. Osmond CB (1978) Crassulacean acid metabolism: a curiosity. Annu Rev Plant Physiol 29:379–414.  https://doi.org/10.1146/annurev.pp.29.060178.002115 Google Scholar
  38. Ouzounis T, Fretté X, Ottosen CO, Rosenqvist E (2015) Spectral effects of LEDs on chlorophyll fluorescence and pigmentation in Phalaenopsis “Vivien” and “Purple Star. Physiol Plant 154:314–327.  https://doi.org/10.1111/ppl.12300 Google Scholar
  39. Pollet B, Steppe K, van Labeke MC, Lemeur R (2009) Diurnal cycle of chlorophyll fluorescence in Phalaenopsis. Photosynthetica 47:309–312.  https://doi.org/10.1007/s11099-009-0048-x Google Scholar
  40. Pollet B, Steppe K, Dambre P, Van Labeke MC, Lemeur R (2010) Seasonal variation of photosynthesis and photosynthetic efficiency in Phalaenopsis. Photosynthetica 48:580–588.  https://doi.org/10.1007/s11099-010-0075-7 Google Scholar
  41. Quiles MJ (2005) Photoinhibition of photosystems I and II using chlorophyll fluorescence measurements. J Biol Educ 39:136–138.  https://doi.org/10.1080/00219266.2005.9655981 Google Scholar
  42. Sæbø A, Krekling T, Appelgren M (1995) Light quality affects photosynthesis and leaf anatomy of birch plantlets in vitro. Plant Cell Tissue Organ Cult 41:177–185.  https://doi.org/10.1007/BF00051588 Google Scholar
  43. Sayed OH (2001) Crassulacean acid metabolism 1975–2000, a Check list. Photosynthetica.  https://doi.org/10.1023/A:1020292623960 Google Scholar
  44. Shengxin C, Chunxia L, Xuyang Y, Song C, Xuelei J, Xiaoying L, Zhigang X, Rongzhan G (2016) Morphological, photosynthetic, and physiological responses of rapeseed leaf to different combinations of red and blue lights at the rosette stage. Front Plant Sci 7:1–12.  https://doi.org/10.3389/fpls.2016.01144 Google Scholar
  45. Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247.  https://doi.org/10.1146/annurev.arplant.57.032905.105434 Google Scholar
  46. Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC (2010) Evolution along the crassulacean acid metabolism continuum. Funct Plant Biol 37:995–1010.  https://doi.org/10.1071/FP10084 Google Scholar
  47. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33:481–518.  https://doi.org/10.1146/annurev.pp.33.060182.002405 Google Scholar
  48. Terashima I, Fujita T, Inoue T, Chow WS, Oguchi R (2009) Green light drives leaf photosynthesis more efficiently than red light in strong white light: Revisiting the enigmatic question of why leaves are green. Plant Cell Physiol 50:684–697.  https://doi.org/10.1093/pcp/pcp034 Google Scholar
  49. Tikkanen M, Grieco M, Kangasjärvi S, Aro E-M (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152:723–735.  https://doi.org/10.1104/pp.109.150250 Google Scholar
  50. Trouwborst G, Hogewoning SW, van Kooten O, Harbinson J, van Ieperen W (2016) Plasticity of photosynthesis after the “red light syndrome” in cucumber. Environ Exp Bot 121:75–82.  https://doi.org/10.1016/j.envexpbot.2015.05.002 Google Scholar
  51. van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150.  https://doi.org/10.1007/BF00033156 Google Scholar
  52. Walters RG, Horton P (1994) Acclimation of Arabidopsis thaliana to the light environment: changes in composition of the photosynthetic apparatus. Planta 195:248–256.  https://doi.org/10.1007/BF00199685 Google Scholar
  53. Winter K, Lesch M (1992) Diurnal changes in chlorophyll a fluorescence and carotenoid composition in Opuntia ficus-indica, a CAM plant, and in three C3 species in Portugal during summer. Oecologia 91:505–510.  https://doi.org/10.1007/BF00650323 Google Scholar
  54. Yang X, Cushman JC, Borland AM, Edwards EJ, Wullschleger SD, Tuskan GA, Owen NA, Griffiths H, Smith JAC, De Paoli HC, Weston DJ, Cottingham R, Hartwell J, Davis SC, Silvera K, Ming R, Schlauch K, Abraham P, Stewart JR, Guo HB, Albion R, Ha J, Lim SD, Wone BWM, Yim WC, Garcia T, Mayer JA, Petereit J, Nair SS, Casey E, Hettich RL, Ceusters J, Ranjan P, Palla KJ, Yin H, Reyes-Garccia C, Andrade JL, Freschi L, Beltran JD, Dever LV, Boxall SF, Waller J, Davies J, Bupphada P, Kadu N, Winter K, Sage RF, Aguilar CN, Schmutz J, Jenkins J, Holtum JAM (2015) A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytol 207:491–504.  https://doi.org/10.1111/nph.13393 Google Scholar
  55. Zheng L, Van Labeke M-C (2017a) Chrysanthemum morphology, photosynthetic efficiency and antioxidant capacity are differentially modified by light quality. J Plant Physiol 213:66–74.  https://doi.org/10.1016/j.jplph.2017.03.005 Google Scholar
  56. Zheng L, Van Labeke M-C (2017b) Long-term effects of red- and blue-light emitting diodes on leaf anatomy and photosynthetic efficiency of three ornamental pot plants. Front Plant Sci 8:1–12.  https://doi.org/10.3389/fpls.2017.00917 Google Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Plants and CropsGhent UniversityGhentBelgium
  2. 2.Department of Biosystems, Division of Crop Biotechnics, Research group for Sustainable Crop Production & ProtectionKU LeuvenGeelBelgium
  3. 3.College of Water Resource and Civil EngineeringChina Agricultural UniversityBeijingPeople’s Republic of China
  4. 4.Centre for Environmental Sciences, Environmental BiologyUHasseltDiepenbeekBelgium

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