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Planta

pp 1–12 | Cite as

Plant biodiversity and regulation of photosynthesis in the natural environment

  • Simone Sello
  • Andrea Meneghesso
  • Alessandro Alboresi
  • Barbara Baldan
  • Tomas MorosinottoEmail author
Original Article

Abstract

Main conclusion

Investigation of photosynthesis regulation in different plant groups exposed to variable conditions showed that all species have similar photosynthetic electron transport modulation while excess energy dissipation is species specific.

Photosynthesis is regulated in response to dynamic environmental conditions to satisfy plant metabolic demands while also avoiding possible over-excitation of the electron transport chain and the generation of harmful reactive oxygen species. Photosynthetic organisms evolved several mechanisms to modulate light harvesting and electron transport efficiency to respond to conditions changing at different timescales, going from fast sun flecks to slow seasonal variations. These regulatory mechanisms changed during evolution of photosynthetic organisms, also adapting to various ecological niches, making the investigation of plant biodiversity highly valuable to uncover conserved traits and plasticity of photosynthetic regulation and complement studies on model species. In this work, a set of plants belonging to different genera of angiosperms, gymnosperms, ferns and lycophytes were investigated by monitoring their photosynthetic parameters in different seasons looking for common trends and differences. In all plants, analysed photosynthetic electron transport rate was found to be modulated by growth light intensity, ensuring a balance between available energy and photochemical capacity. Growth light also influenced the threshold where heat dissipation of excitation energy, a mechanism called non-photochemical quenching (NPQ), was activated. On the contrary, NPQ amplitude did not correlate with light intensity experienced by the plants but was a species-specific feature. The zeaxanthin-dependent component of NPQ, qZ, was found to be the most variable in different plants and its modulation influenced the intensity and the kinetic properties of the response.

Keywords

Photosynthesis Acclimation Non-photochemical quenching Photoprotection Plant biodiversity 

Notes

Acknowledgements

We would like to thank Botanical Garden of Padova personnel and in particular Roberto Tacchetto and Simone Mazzucato for their support during sampling and measurements.

Supplementary material

425_2018_3077_MOESM1_ESM.pdf (786 kb)
Supplementary material 1 (pdf 785 kb)

References

  1. Alboresi A, Storti M, Morosinotto T (2018) Balancing protection and efficiency in the regulation of photosynthetic electron transport across plant evolution. New Phytol.  https://doi.org/10.1111/nph.15372 Google Scholar
  2. Allahverdiyeva Y, Suorsa M, Tikkanen M, Aro E-ME-M (2015) Photoprotection of photosystems in fluctuating light intensities. J Exp Bot 66:2427–2436.  https://doi.org/10.1093/jxb/eru463 CrossRefGoogle Scholar
  3. Arnoux P, Morosinotto T, Saga G et al (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21:2036–2044.  https://doi.org/10.1105/tpc.109.068007 CrossRefGoogle Scholar
  4. Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958.  https://doi.org/10.1074/jbc.M606417200 CrossRefGoogle Scholar
  5. Bernardi A, Nikolaou A, Meneghesso A et al (2016) High-fidelity modelling methodology of light-limited photosynthetic production in microalgae. PLoS ONE 11:e0152387.  https://doi.org/10.1371/journal.pone.0152387 CrossRefGoogle Scholar
  6. Chaw SM, Parkinson CL, Cheng Y et al (2000) Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc Natl Acad Sci USA 97:4086–4091.  https://doi.org/10.1073/PNAS.97.8.4086 CrossRefGoogle Scholar
  7. Dall’Osto L, Cazzaniga S, Wada M, Bassi R (2014) On the origin of a slowly reversible fluorescence decay component in the Arabidopsis npq4 mutant. Philos Trans R Soc Lond B Biol Sci 369:20130221.  https://doi.org/10.1098/rstb.2013.0221 CrossRefGoogle Scholar
  8. Demmig-Adams B, Ebbert V, Mellman DL et al (2006) Modulation of PsbS and flexible vs sustained energy dissipation by light environment in different species. Physiol Plant 127:670–680.  https://doi.org/10.1111/j.1399-3054.2006.00698.x CrossRefGoogle Scholar
  9. Eberhard S, Finazzi G, Wollman F-A (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515.  https://doi.org/10.1146/annurev.genet.42.110807.091452 CrossRefGoogle Scholar
  10. Ferroni L, Cucuzza S, Angeleri M et al (2017) In the lycophyte Selaginella martensii is the “extra-qT” related to energy spillover? Insights into photoprotection in ancestral vascular plants. Environ Exp Bot.  https://doi.org/10.1016/j.envexpbot.2017.10.023 Google Scholar
  11. Gerotto C, Morosinotto T (2013) Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS-dependent NPQ in late Streptophyte algae. Physiol Plant 149:583–598.  https://doi.org/10.1111/ppl.12070 CrossRefGoogle Scholar
  12. Gerotto C, Alboresi A, Giacometti GMGM et al (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932.  https://doi.org/10.1111/j.1365-3040.2011.02294.x CrossRefGoogle Scholar
  13. Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci 96:8762–8767.  https://doi.org/10.1073/pnas.96.15.8762 CrossRefGoogle Scholar
  14. Holzwarth AR, Lenk D, Jahns P (2013) On the analysis of non-photochemical chlorophyll fluorescence quenching curves: I Theoretical considerations. Biochim Biophys Acta 1827:786–792.  https://doi.org/10.1016/j.bbabio.2013.02.011 CrossRefGoogle Scholar
  15. Huner N, Oquist G, Hurry V (1993) Photoinhibition and low-temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39CrossRefGoogle Scholar
  16. Ilík P, Pavlovič A, Kouřil R et al (2017) Alternative electron transport mediated by flavodiiron proteins is operational in organisms from cyanobacteria up to gymnosperms. New Phytol.  https://doi.org/10.1111/nph.14536 Google Scholar
  17. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322.  https://doi.org/10.1073/pnas.1110189108 CrossRefGoogle Scholar
  18. Jung H-S, Niyogi KK (2009) Quantitative genetic analysis of thermal dissipation in Arabidopsis. Plant Physiol 150:977–986.  https://doi.org/10.1104/pp.109.137828 CrossRefGoogle Scholar
  19. Kromdijk J, Głowacka K, Leonelli L et al (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:857–861.  https://doi.org/10.1126/science.aai8878 CrossRefGoogle Scholar
  20. Kulheim C, Agren J, Jansson S et al (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93.  https://doi.org/10.1126/science.1072359 CrossRefGoogle Scholar
  21. Larosa V, Meneghesso A, La Rocca N et al (2018) mitochondria affect photosynthetic electron transport and photosensitivity in a green alga. Plant Physiol 176:2305–2314.  https://doi.org/10.1104/pp.17.01249 CrossRefGoogle Scholar
  22. Li XP, Björkman O, Shih C et al (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395.  https://doi.org/10.1038/35000131 CrossRefGoogle Scholar
  23. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260.  https://doi.org/10.1146/annurev.arplant.58.032806.103844 CrossRefGoogle Scholar
  24. Lu Y, Ran J-H, Guo D-M et al (2014) Phylogeny and divergence times of gymnosperms inferred from single-copy nuclear genes. PLoS ONE 9:e107679.  https://doi.org/10.1371/journal.pone.0107679 CrossRefGoogle Scholar
  25. Malnoë A (2018) Photoinhibition or photoprotection of photosynthesis? Update on the (newly termed) sustained quenching component qH. Environ Exp Bot 154:123–133.  https://doi.org/10.1016/j.envexpbot.2018.05.005 CrossRefGoogle Scholar
  26. Malnoë A, Schultink A, Shahrasbi S et al (2018) The plastid lipocalin LCNP is required for sustained photoprotective energy dissipation in Arabidopsis. Plant Cell 30:196–208.  https://doi.org/10.1105/tpc.17.00536 CrossRefGoogle Scholar
  27. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  28. Miyake C, Horiguchi S, Makino A et al (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830.  https://doi.org/10.1093/pcp/pci197 CrossRefGoogle Scholar
  29. Nilkens M, Kress E, Lambrev P et al (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophys Acta 1797:466–475.  https://doi.org/10.1016/j.bbabio.2010.01.001 CrossRefGoogle Scholar
  30. Oakley CG, Savage L, Lotz S et al (2018) Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana. J Exp Bot 69:699–709.  https://doi.org/10.1093/jxb/erx437 CrossRefGoogle Scholar
  31. Peers G, Truong TB, Ostendorf E et al (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521.  https://doi.org/10.1038/nature08587 CrossRefGoogle Scholar
  32. Peltier G, Tolleter D, Billon E, Cournac L (2010) Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth Res 106:19–31.  https://doi.org/10.1007/s11120-010-9575-3 CrossRefGoogle Scholar
  33. Peltier G, Aro E-M, Shikanai T (2016) NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annu Rev Plant Biol 67:55–80.  https://doi.org/10.1146/annurev-arplant-043014-114752 CrossRefGoogle Scholar
  34. Shimakawa G, Murakami A, Niwa K et al (2018) Comparative analysis of strategies to prepare electron sinks in aquatic photoautotrophs. Photosynth Res.  https://doi.org/10.1007/s11120-018-0522-z Google Scholar
  35. Shubin VV, Terekhova IN, Kirillov BA, Karapetyan NV (2008) Quantum yield of P700+ photodestruction in isolated photosystem I complexes of the cyanobacterium Arthrospira platensis. Photochem Photobiol Sci 7:956–962.  https://doi.org/10.1039/b719122g CrossRefGoogle Scholar
  36. Soltis DE, Smith SA, Cellinese N et al (2011) Angiosperm phylogeny: 17 genes, 640 taxa. Am J Bot 98:704–730.  https://doi.org/10.3732/ajb.1000404 CrossRefGoogle Scholar
  37. Takagi D, Ishizaki K, Hanawa H et al (2017) Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I. Physiol Plant 161:56–74.  https://doi.org/10.1111/ppl.12562 CrossRefGoogle Scholar
  38. Tiwari A, Mamedov F, Grieco M et al (2016) Photodamage of iron–sulphur clusters in photosystem I induces non-photochemical energy dissipation. Nat Plants.  https://doi.org/10.1038/nplants.2016.35 Google Scholar
  39. Vasco A, Moran RC, Ambrose BA (2013) The evolution, morphology, and development of fern leaves. Front Plant Sci 4:345.  https://doi.org/10.3389/fpls.2013.00345 CrossRefGoogle Scholar
  40. Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447.  https://doi.org/10.1093/jxb/eri060 CrossRefGoogle Scholar
  41. Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67:81–106.  https://doi.org/10.1146/annurev-arplant-043015-112002 CrossRefGoogle Scholar
  42. Yin Q, Wang L, Lei M et al (2017) The relationships between leaf economics and hydraulic traits of woody plants depend on water availability. Sci Total Environ 621:245–252.  https://doi.org/10.1016/j.scitotenv.2017.11.171 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of PadovaPaduaItaly
  2. 2.Botanical GardenUniversity of PadovaPaduaItaly

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