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RESEARCH ARTICLE
Contents Vol 51(10)

Differential modulation of photosystem II photochemical efficiency in six C4 xero-halophytes

Ahmad Zia https://orcid.org/0000-0002-9263-4873 A * , Salman Gulzar B and Gerald E. Edwards C
+ Author Affiliations
- Author Affiliations

A Department of Biology, University of Hafr Al-Batin, Hafr Al-Batin 31991, Saudi Arabia.

B Institute of Sustainable Halophyte Utilization, University of Karachi, Karachi 75270, Pakistan.

C School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA.

* Correspondence to: ahmad.zia1@outlook.com, ahmadzia@uhb.edu.sa

Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 51, FP24060 https://doi.org/10.1071/FP24060
Submitted: 28 February 2024  Accepted: 18 September 2024  Published: 4 October 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Xero-halophytes are the salt-tolerant plants of dry habitats that adapt efficient strategies to endure extreme salt and water fluctuations. This study elucidated the adaptations related to PSII photochemistry, photoprotection, and photoinhibition in six C4 xero-halophytes (Atriplex stocksii, Haloxylon stocksii, Salsola imbricata, Suaeda fruticosa, Desmostachya bipinnata, and Saccharum griffithii) grown in their native habitats. Chlorophyll a fluorescence quenching measurements suggested that S. imbricata and H. stocksii maintained efficient PSII photochemistry by downregulating heat dissipation and keeping a high fraction of open PSII centres that indicates plastoquinone (PQ) pool oxidation. Fluorescence induction kinetics revealed that S. imbricata demonstrated the highest performance index of PSII excitation to the reduction of end electron acceptors. S. fruticosa sustained photochemical efficiency through enhanced dissipation of excess energy and a low fraction of open PSII centres, indicating PQ reduced state. The large light-harvesting antenna size, deduced from the chlorophyll a/b ratio in S. fruticosa apparently led to the superior performance index of PSII excitation to the reduction of intersystem electron carriers. A. stocksii retained more open PSII centres with responsive non-photochemical quenching to safely dissipate excess energy. Despite maintaining the highest pigment contents and stoichiometry, A. stocksii remained lowest in both performance indices. The grass species D. bipinnata and S. griffithii kept fewer PSII centres open during photoinhibition, as evidenced by downregulation of PSII operating efficiency. The results provide insights into the differential modulation of PSII photochemical efficiency through dynamic control of photoprotective energy dissipation, PQ pool redox states, and photoinhibitory shutdown in these xero-halophytes.

Keywords: C4 Xero-halophytes, chlorophyll a fluorescence, non-photochemical quenching, photochemical efficiency, photoprotection, photosynthetic pigments, photosystem II, plastoquinone redox, salinity stress.

References

Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1143, 113-134.
| Crossref | Google Scholar | PubMed |

Bacarin MA, Martinazzo EG, Cassol D, Falqueto AR, Silva DM (2016) Daytime variations of chlorophyll a fluorescence in pau d’alho seedlings. Revista Árvore 40, 1023-1030.
| Crossref | Google Scholar |

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89-113.
| Crossref | Google Scholar | PubMed |

Bassi R, Dall’Osto L (2021) Dissipation of light energy absorbed in excess: the molecular mechanisms. Annual Review of Plant Biology 72, 47-76.
| Crossref | Google Scholar | PubMed |

Cope TA (1982) Poaceae. In ‘Flora of Pakistan’. (Eds E Nasir, SI Ali) p. 678. (University of Karachi: Pakistan)

Demmig B, Winter K, Krüger A, Czygan F-C (1987) Photoinhibition and zeaxanthin formation in intact leaves: a possible role of the xanthophyll cycle in the dissipation of excess light energy. Plant Physiology 84, 218-224.
| Crossref | Google Scholar | PubMed |

Duarte B, Santos D, Marques JC, Caçador I (2013) Ecophysiological adaptations of two halophytes to salt stress: photosynthesis, PS II photochemistry and anti-oxidant feedback – implications for resilience in climate change. Plant Physiology and Biochemistry 67, 178-188.
| Crossref | Google Scholar | PubMed |

Freschet GT, Dias ATC, Ackerly DD, Aerts R, van Bodegom PM, Cornwell WK, Dong M, Kurokawa H, Liu G, Onipchenko VG, et al. (2011) Global to community scale differences in the prevalence of convergent over divergent leaf trait distributions in plant assemblages. Global Ecology and Biogeography 20, 755-765.
| Crossref | Google Scholar |

Guidi L, Lo Piccolo E, Landi M (2019) Chlorophyll fluorescence, photoinhibition and abiotic stress: does it make any difference the fact to be a C3 or C4 species? Frontiers in Plant Science 10, 174.
| Crossref | Google Scholar | PubMed |

Johnson MP, Zia A, Horton P, Ruban AV (2010) Effect of xanthophyll composition on the chlorophyll excited state lifetime in plant leaves and isolated LHCII. Chemical Physics 373, 23-32.
| Crossref | Google Scholar |

Kajala K, Covshoff S, Karki S, Woodfield H, Tolley BJ, Dionora MJA, Mogul RT, Mabilangan AE, Danila FR, Hibberd JM, Quick WP (2011) Strategies for engineering a two-celled C4 photosynthetic pathway into rice. Journal of Experimental Botany 62, 3001-3010.
| Crossref | Google Scholar | PubMed |

Kalaji HM, Govindjee , Bosa K, Kościelniak J, Żuk-Gołaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany 73, 64-72.
| Crossref | Google Scholar |

Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Lukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum 38, 102.
| Crossref | Google Scholar |

Kalaji HM, Račková L, Paganová V, Swoczyna T, Rusinowski S, Sitko K (2018) Can chlorophyll-a fluorescence parameters be used as bio-indicators to distinguish between drought and salinity stress in Tilia cordata Mill? Environmental and Experimental Botany 152, 149-157.
| Crossref | Google Scholar |

Khorobrykh SA, Karonen M, Tyystjärvi E (2015) Experimental evidence suggesting that H2O2 is produced within the thylakoid membrane in a reaction between plastoquinol and singlet oxygen. FEBS Letters 589, 779-786.
| Crossref | Google Scholar | PubMed |

Killi D, Bussotti F, Raschi A, Haworth M (2017) Adaptation to high temperature mitigates the impact of water deficit during combined heat and drought stress in C3 sunflower and C4 maize varieties with contrasting drought tolerance. Physiologia Plantarum 159, 130-147.
| Crossref | Google Scholar | PubMed |

Koyro H-W, Hussain T, Huchzermeyer B, Khan MA (2013) Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations. Environmental and Experimental Botany 91, 22-29.
| Crossref | Google Scholar |

Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209-218.
| Crossref | Google Scholar | PubMed |

Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857-861.
| Crossref | Google Scholar | PubMed |

Kubásek J, Urban O, Šantrůček J (2013) C4 plants use fluctuating light less efficiently than do C3 plants: a study of growth, photosynthesis and carbon isotope discrimination. Physiologia Plantarum 149, 528-539.
| Crossref | Google Scholar | PubMed |

Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry 1, F4.3.1-F4.3.8.
| Crossref | Google Scholar |

Lichtenthaler HK, Buschmann C, Döll M, Fietz H-J, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynthesis Research 2, 115-141.
| Crossref | Google Scholar | PubMed |

Marchesini VA, Yin C, Colmer TD, Veneklaas EJ (2014) Drought tolerances of three stem-succulent halophyte species of an inland semiarid salt lake system. Functional Plant Biology 41(12), 1230-1238.
| Crossref | Google Scholar | PubMed |

Miyake C, Amako K, Shiraishi N, Sugimoto T (2009) Acclimation of tobacco leaves to high light intensity drives the plastoquinone oxidation system – relationship among the fraction of open PSII centers, non-photochemical quenching of Chl fluorescence and the maximum quantum yield of PSII in the dark. Plant and Cell Physiology 50, 730-743.
| Crossref | Google Scholar | PubMed |

Moinuddin M, Gulzar S, Hameed A, Gul B, Ajmal Khan M, Edwards GE (2017) Differences in photosynthetic syndromes of four halophytic marsh grasses in Pakistan. Photosynthesis Research 131, 51-64.
| Crossref | Google Scholar | PubMed |

Murata N, Miyao M (1985) Extrinsic membrane proteins in the photosynthetic oxygen-evolving complex. Trends in Biochemical Sciences 10, 122-124.
| Crossref | Google Scholar |

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1767, 414-421.
| Crossref | Google Scholar | PubMed |

Niyogi KK, Grossman AR, Björkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121-1134.
| Crossref | Google Scholar | PubMed |

Oukarroum A, Bussotti F, Goltsev V, Kalaji HM (2015) Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress. Environmental and Experimental Botany 109, 80-88.
| Crossref | Google Scholar |

Pfündel E (1998) Estimating the contribution of Photosystem I to total leaf chlorophyll fluorescence. Photosynthesis Research 56, 185-195.
| Crossref | Google Scholar |

Pokorska B, Romanowska E (2007) Photoinhibition and D1 protein degradation in mesophyll and agranal bundle sheath thylakoids of maize. Functional Plant Biology 34, 844-852.
| Crossref | Google Scholar | PubMed |

Romanowska E, Buczyńska A, Wasilewska W, Krupnik T, Drożak A, Rogowski P, Parys E, Zienkiewicz M (2017) Differences in photosynthetic responses of NADP-ME type C4 species to high light. Planta 245, 641-657.
| Crossref | Google Scholar | PubMed |

Rotasperti L, Tadini L, Chiara M, Crosatti C, Guerra D, Tagliani A, Forlani S, Ezquer I, Horner DS, Jahns P, et al. (2022) The barley mutant happy under the sun 1 (hus1): an additional contribution to pale green crops. Environmental and Experimental Botany 196, 104795.
| Crossref | Google Scholar |

Sage RF, Sultmanis S (2016) Why are there no C4 forests? Journal of Plant Physiology 203, 55-68.
| Crossref | Google Scholar | PubMed |

Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annual Review of Plant Biology 63, 19-47.
| Crossref | Google Scholar | PubMed |

Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1706, 250-261.
| Crossref | Google Scholar | PubMed |

Serôdio J, Campbell DA (2021) Photoinhibition in optically thick samples: Effects of light attenuation on chlorophyll fluorescence-based parameters. Journal of Theoretical Biology 513, 110580.
| Crossref | Google Scholar |

Shuyskaya E, Rakhmankulova Z, Prokofieva M, Saidova L, Toderich K, Voronin P (2022) Intensity and duration of salinity required to form adaptive response in C4 halophyte Kochia prostrata (L.) Shrad. Frontiers in Plant Science 13, 955880.
| Crossref | Google Scholar | PubMed |

Sipka G, Magyar M, Mezzetti A, Akhtar P, Zhu Q, Xiao Y, Han G, Santabarbara S, Shen J-R, Lambrev P, Garab G (2021) Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center. The Plant Cell 33, 1286-1302.
| Crossref | Google Scholar |

Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynthesis Research 113, 15-61.
| Crossref | Google Scholar | PubMed |

Stirbet A, Riznichenko GY, Rubin AB, Govindjee (2014) Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry (Moscow) 79, 291-323.
| Crossref | Google Scholar | PubMed |

Stirbet A, Lazár D, Kromdijk J, Govindjee (2018) Chlorophyll a fluorescence induction: can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica 56, 86-104.
| Crossref | Google Scholar |

Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In ‘Probing photosynthesis: mechanisms, regulation and adaptation’. (Eds M Yunus, U Pathre, P Mohanty) pp. 445–483. (Taylor and Francis: London, UK)

Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In ‘Chlorophyll a fluorescence, a signature of photosynthesis’. Advances in Photosynthesis and Respiration’. (Eds GC Papageorgiou, Govindjee) pp. 321–362. (Springer: Dordrecht, Netherlands)

Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1797, 1313-1326.
| Crossref | Google Scholar | PubMed |

Sun Q, Yamada T, Han Y, Takano T (2021) Influence of salt stress on C4 photosynthesis in Miscanthus sinensis Anderss. Plant Biology 23(1), 44-56.
| Crossref | Google Scholar | PubMed |

Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends in Plant Science 13, 178-182.
| Crossref | Google Scholar | PubMed |

Tikkanen M, Aro E-M (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1817, 232-238.
| Crossref | Google Scholar | PubMed |

Tikkanen M, Mekala NR, Aro E-M (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1837, 210-215.
| Crossref | Google Scholar | PubMed |

Wungrampha S, Joshi R, Rathore RS, Singla-Pareek SL, Govindjee , Pareek A (2019) CO2 uptake and chlorophyll a fluorescence of Suaeda fruticosa grown under diurnal rhythm and after transfer to continuous dark. Photosynthesis Research 142, 211-227.
| Crossref | Google Scholar | PubMed |

Zia A, Johnson MP, Ruban AV (2011) Acclimation- and mutation-induced enhancement of PsbS levels affects the kinetics of non-photochemical quenching in Arabidopsis thaliana. Planta 233, 1253-1264.
| Crossref | Google Scholar | PubMed |

Zia A, Walker BJ, Oung HMO, Charuvi D, Jahns P, Cousins AB, Farrant JM, Reich Z, Kirchhoff H (2016) Protection of the photosynthetic apparatus against dehydration stress in the resurrection plant Craterostigma pumilum. The Plant Journal 87, 664-680.
| Crossref | Google Scholar | PubMed |

Zia A, Hegazy HS, Hassan NS, Naguib DM, Abdel-Haliem MEF (2021) Biochemical responses of wheat to silicon application under salinity. Journal of Plant Nutrition and Soil Science 184, 255-262.
| Crossref | Google Scholar |

Zia A, Gulzar S, Ruban AV (2024) Enhanced photochemical efficiency of PSII in Prosopis juliflora suggests contribution to invasion advantage over native C3 xero-halophytes under salt stress. Functional Plant Biology 51, FP23272.
| Crossref | Google Scholar |

Zivcak M, Brestic M, Kunderlikova K, Olsovska K, Allakhverdiev SI (2015) Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: does activity of photosystem I play any role in OJIP rise? Journal of Photochemistry and Photobiology B: Biology 152, 318-324.
| Crossref | Google Scholar | PubMed |