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Plant function and evolutionary biology
RESEARCH ARTICLE

Functional variations in efficiency of PSII during leaf ontogeny in the tropical plant Saraca asoca

  Shasmita https://orcid.org/0000-0002-2152-6576 A B , Barsha Bhushan Swain https://orcid.org/0000-0002-8988-1232 A , Smrutirekha Mishra https://orcid.org/0000-0003-0180-6033 A , Debasish Mohapatra https://orcid.org/0000-0002-1430-9979 A , Soumendra Kumar Naik https://orcid.org/0000-0002-3479-6911 A and Pradipta Kumar Mohapatra https://orcid.org/0000-0001-7435-7983 A *
+ Author Affiliations
- Author Affiliations

A Department of Botany, Ravenshaw University, Cuttack, Odisha 753003, India. Email: shasmitahota@ymail.com, barsha.bhushan.swain@gmail.com, smrutirekhamishra08@gmail.com, debasish2050@gmail.com, sknuu@yahoo.com, pradiptamoha@yahoo.com

B PG Department of Botany, Dhenkanal Autonomous College, Dhenkanal, Odisha 759001, India.

* Correspondence to: pradiptamoha@yahoo.com

Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 51, FP24176 https://doi.org/10.1071/FP24176
Submitted: 1 July 2024  Accepted: 3 September 2024  Published: 19 September 2024

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

Abstract

Leaf ontogeny of tropical evergreen tree species lasts several months with changes in size, shape, colouration and internal tissue distribution of leaves. Leaf initiation in Saraca asoca generally occurs once in a year during February–April, followed by very limited leafing thereafter. We measured the rate of photosynthesis, chlorophyll a fluorescence, energy quenching and PSII functions during the leaf ontogeny process. Observations were taken up to 35 days after opening of lamina (DAOL). Significant increase in the synthesis and accumulation of photosynthetic pigments but negative net photosynthesis was noticed during initial days of the ontogeny. The leaf moved from heterotrophy to autotrophy with gradual improvement of PSII functions. The ratio of intercellular CO2 (Ci) and ambient CO2 (Ca) showed significant change at ≥11 DAOL. Increase in the age of the leaf (between 5 and 28 DAOL) caused decrease in O-J rise and corresponding increase in J-I and I-P rise as well as of fluorescence maximum (FM) of the OJIP curve. The improvement of the electron transport components of the donor side of PSII was seen with increase in the functional oxygen evolving complex. The functional improvements of the donor and acceptor side of PSII during leaf ontogeny are discussed.

Keywords: chlorophyll a fluorescence, electron transport, photochemical quenching, photosynthesis, photosystem II, Saraca asoca, stomatal conductance, transpiration.

References

Bauerle WL, McCullough C, Iversen M, Hazlett M (2020) Leaf age and position effects on quantum yield and photosynthetic capacity in hemp crowns. Plants 9(2), 271.
| Crossref | Google Scholar |

Bielczynski LW, Łącki MK, Hoefnagels I, Gambin A, Croce R (2017) Leaf and plant age affects photosynthetic performance and photoprotective capacity. Plant Physiology 175, 1634-1648.
| Crossref | Google Scholar |

Bird T, Nestor BJ, Bayer PE, Wang G, Ilyasova A, Gille CE, Soraru BEH, Ranathunge K, Severn-Ellis AA, Jost R, Scheible W-R, Dassanayake M, Batley J, Edwards D, Lambers H, Finnegan PM (2024) Delayed leaf greening involves a major shift in the expression of cytosolic and mitochondrial ribosomes to plastid ribosomes in the highly phosphorus-use-efficient Hakea prostrata (Proteaceae). Plant and Soil 496, 7-30.
| Crossref | Google Scholar |

Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji HM, Allakhverdiev SI (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynthesis Research 125, 151-166.
| Crossref | Google Scholar |

Cai ZQ, Slot M, Fan ZX (2005) Leaf development and photosynthetic properties of three tropical tree species with delayed greening. Photosynthetica 43, 91-98.
| Crossref | Google Scholar |

Choinski JS, Jr, Ralph P, Eamus D (2003) Changes in photosynthesis during leaf expansion in Corymbia gummifera. Australian Journal of Botany 51, 111-118.
| Crossref | Google Scholar |

Chondrogiannis C, Grammatikopoulos G (2016) Photosynthesis in developing leaf of juveniles and adults of three Mediterranean species with different growth forms. Photosynthesis Research 130, 427-444.
| Crossref | Google Scholar |

Claßen-Bockhoff R, Franke D, Krähmer H (2021) Early ontogeny defines the diversification of primary vascular bundle systems in angiosperms. Botanical Journal of the Linnean Society 195, 281-307.
| Crossref | Google Scholar |

Detto M, Xu X (2020) Optimal leaf life strategies determine Vc,max dynamic during ontogeny. New Phytologist 228, 361-375.
| Crossref | Google Scholar |

Dodd IC, Critchley C, Woodall GS, Stewart GR (1998) Photoinhibition in differently coloured juvenile leaves of Syzygium species. Journal of Experimental Botany 49, 1437-1445.
| Crossref | Google Scholar |

Flexas J, Carriquí M (2020) Photosynthesis and photosynthetic efficiencies along the terrestrial plant’s phylogeny: lessons for improving crop photosynthesis. The Plant Journal 101, 964-978.
| Crossref | Google Scholar |

Force L, Critchley C, van Rensen JJS (2003) New fluorescence parameters for monitoring photosynthesis in plants. Photosynthesis Research 78(1), 17-33.
| Crossref | Google Scholar |

Fu X, Zhang J, Zhou L, Mo W, Wang H, Huang X (2022) Characterizing the development of photosynthetic capacity in relation to chloroplast structure and mineral nutrition in leaves of three woody fruit species. Tree Physiology 42, 989-1001.
| Crossref | Google Scholar |

Gao J, Li P, Ma F, Goltsev V (2014) Photosynthetic performance during leaf expansion in Malus micromalus probed by chlorophyll a fluorescence and modulated 820 nm reflection. Journal of Photochemistry and Photobiology B: Biology 137, 144-150.
| Crossref | Google Scholar |

Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) – General Subjects 990, 87-92.
| Crossref | Google Scholar |

Giorio P, Sellami MH (2021) Polyphasic OKJIP chlorophyll a fluorescence transient in a landrace and a commercial cultivar of sweet pepper (Capsicum annuum, L.) under long-term salt stress. Plants 10, 887.
| Crossref | Google Scholar |

Gomez KA, Gomez AA (1984) ‘Statistical procedures for agricultural research.’ 2nd edn. (John Wiley & Sons: New York, NY USA)

Gonzalez-Paleo L, Ravetta DA (2018) Relationship between photosynthetic rate, water use and leaf structure in desert annual and perennial forbs differing in their growth. Photosynthetica 56, 1177-1187.
| Crossref | Google Scholar |

Han J, Lei Z, Flexas J, Zhang Y, Carriquí M, Zhang W, Zhang Y (2018) Mesophyll conductance in cotton bracts: anatomically determined internal CO2 diffusion constraints on photosynthesis. Journal of Experimental Botany 69, 5433-5443.
| Crossref | Google Scholar |

Hassan S, Ahmad A, Batool F, Rashid B, Husnain T (2021) Genetic modification of Gossypium arboreum universal stress protein (GUSP1) improves drought tolerance in transgenic cotton (Gossypium hirsutum). Physiology and Molecular Biology of Plants 27, 1779-1794.
| Crossref | Google Scholar |

IUCN (2021) IUCN red list of threatened species. Version 2021.1. Available at www.iucnredlist.org

Jiang CD, Shi L, Gao HY, Schansker G, Toth SZ, Strasser RJ (2006) Development of photosystems 2 and 1 during leaf growth in grapevine seedlings probed by chlorophyll a fluorescence transient and 820 nm transmission in vivo. Photosynthetica 44, 454-463.
| Crossref | Google Scholar |

Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik 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 |

Kalve S, De Vos D, Beemster GTS (2014) Leaf development: a cellular perspective. Frontiers in Plant Science 5, 362.
| Crossref | Google Scholar |

Krause GH, Virgo A, Winter K (1995) High susceptibility to photoinhibition of young leaves of tropical forest trees. Planta 197, 583-591.
| Crossref | Google Scholar |

Kursar TA, Coley PD (1992) Delayed development of the photosynthetic apparatus in tropical rain forest species. Functional Ecology 6, 411-422.
| Crossref | Google Scholar |

Lan J-X, Li A-L, Chen C-X (2011) Effect of transient accumulation of anthocyanin on leaf development and photoprotection of Fagopyrum dibotrys mutant. Biologia plantarum 55, 766-770.
| Crossref | Google Scholar |

Leister D (2023) Enhancing the light reactions of photosynthesis: strategies, controversies, and perspectives. Molecular Plant 16, 4-22.
| Crossref | Google Scholar |

Liao C, Shen H, Gao Z, Wang Y, Zhu Z, Xie Q, Wu T, Chen G, Hu Z (2024) Overexpression of SlCRF6 in tomato inhibits leaf development and affects plant morphology. Plant Science 338, 111921.
| Crossref | Google Scholar |

Maayan I, Shaya F, Ratner K, Mani Y, Lavee S, Avidan B, Shahak Y, Ostersetzer-Biran O (2008) Photosynthetic activity during olive (Olea europaea) leaf development correlates with plastid biogenesis and rubisco levels. Physiologia Plantarum 134, 547-558.
| Crossref | Google Scholar |

Manetas Y, Drinia A, Petropoulou Y (2002) High contents of anthocyanins in young leaves are correlated with low pools of xanthophyll cycle components and low risk of photoinhibition. Photosynthetica 40, 349-354.
| Crossref | Google Scholar |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659-668.
| Crossref | Google Scholar |

Menezes J, Garcia S, Grandis A, Nascimento H, Domingues TF, Guedes AV, Aleixo I, Camargo P, Campos J, Damasceno A, Dias-Silva R, Fleischer K, Kruijt B, Cordeiro AL, Martins NP, Meir P, Norby RJ, Pereira I, Portela B, Rammig A, Ribeiro AG, Lapola DM, Quesada CA (2022) Changes in leaf functional traits with leaf age: when do leaves decrease their photosynthetic capacity in Amazonian trees? Tree Physiology 42, 922-938.
| Crossref | Google Scholar |

Miyazawa S-I, Terashima I (2001) Slow development of leaf photosynthesis in an evergreen broad-leaved tree, Castanopsis sieboldii: relationships between leaf anatomical characteristics and photosynthetic rate. Plant, Cell & Environment 24, 279-291.
| Crossref | Google Scholar |

Mohapatra PK, Swain BB, Mishra S (2023) Govindjee: one of the major architects for the conceptual evolution of the z-scheme of photosynthesis. LS – International Journal of Life Sciences 12, 21-43.
| Crossref | Google Scholar |

Munns R, Millar AH (2023) Seven plant capacities to adapt to abiotic stress. Journal of Experimental Botany 74, 4308-4323.
| Crossref | Google Scholar |

Niinemets Ü, Díaz-Espejo A, Flexas J, Galmés J, Warren CR (2009) Importance of mesophyll diffusion conductance in estimation of plant photosynthesis in the field. Journal of Experimental Botany 60, 2271-2282.
| Crossref | Google Scholar |

Niinemets Ü, García-Plazaola JI, Tosens T (2012) Photosynthesis during leaf development and ageing. In ‘Terrestrial photosynthesis in a changing environment: a molecular, physiological and ecological approach’. (Eds J Flexas, F Loreto, H Medrano) pp. 353–372. (Cambridge University Press: Cambridge, UK) doi:10.1017/CBO9781139051477.028

Ölçer H, Lloyd JC, Raines CA (2001) Photosynthetic capacity is differentially affected by reductions in sedoheptulose-1,7-bisphosphatase activity during leaf development in transgenic tobacco plants. Plant Physiology 125, 982-989.
| Crossref | Google Scholar |

Panda D, Mohanty B, Behera PK, Barik J, Mishra SS (2020) Harnessing leaf photosynthetic traits and antioxidant defence for multiple stress tolerance in three premium indigenous rice landraces of Jeypore tract of Odisha, India. Functional Plant Biology 47, 99-111.
| Crossref | Google Scholar | PubMed |

Papageorgiou GC, Govindjee (2014) The non-photochemical quenching of the electronically excited state of chlorophyll a in plants: definitions, timelines, viewpoints, open questions. In ‘Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria, Vol. 40’. Advances in Photosynthesis and Respiration’. (Eds B Demmig-Adams, G Garab, W Adams III, Govindjee) pp. 1–44. (Springer: Dordrecht, Netherlands) doi:10.1007/978-94-017-9032-1_1

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta (BBA) – Bioenergetics 975, 384-394.
| Crossref | Google Scholar |

Qian X, Liu L, Croft H, Chen J (2021) Relationship between leaf maximum carboxylation rate and chlorophyll content preserved across 13 species. Journal of Geophysical Research: Biogeosciences 126, e2020JG006076.
| Crossref | Google Scholar |

Rho H, Yu DJ, Kim SJ, Chun C, Lee HJ (2011) Estimation of carboxylation efficiency from net CO2 assimilation rate as a function of chloroplastic CO2 concentration in strawberry (Fragaria × ananassa cv. Maehyang) leaves. Horticulture, Environment, and Biotechnology 52, 547-552.
| Crossref | Google Scholar |

Sasi JM, Gupta S, Singh A, Kujur A, Agarwal M, Agarwal SK (2022) Know when and how to die: gaining insights into the molecular regulation of leaf senescence. Physiology and Molecular Biology of Plants 28, 1515-1534.
| Crossref | Google Scholar |

Schaffer B, Whiley AW, Kohli RR (1991) Effects of leaf age on gas exchange characteristics of avocado (Persea americana Mill.). Scientia Horticulturae 48, 21-28.
| Crossref | Google Scholar |

Schlüter U, Colmsee C, Scholz U, Bräutigam A, Weber APM, Zellerhoff N, Bucher M, Fahnenstich H, Sonnewald U (2013) Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balance. BMC Genomics 14, 442.
| Crossref | Google Scholar |

Šesták Z (1985) Chlorophylls and carotenoids during leaf ontogeny. In ‘Photosynthesis during leaf development, Vol. 11’. Tasks for Vegetation Science. (Ed. Z Šestăk) pp. 76–106. (Springer: Dordrecht, Netherlands) doi:10.1007/978-94-009-5530-1_4

Shasmita , Mohapatra D, Mohapatra PK, Naik SK, Mukherjee AK (2019) Priming with salicylic acid induces defense against bacterial blight disease by modulating rice plant photosystem II and antioxidant enzymes activity. Physiological and Molecular Plant Pathology 108, 101427.
| Crossref | Google Scholar |

Silva JRdJ, Cairo PAR, do Bomfim RAA, Barbosa MP, Souza MO, Leite TC (2020) Morphological and physiological changes during leaf ontogeny in genotypes of Eucalyptus young plants. Trees 34, 759-769.
| Crossref | Google Scholar |

Simkin AJ, López-Calcagno PE, Raines CA (2019) Feeding the world: improving photosynthetic efficiency for sustainable crop production. Journal of Experimental Botany 70, 1119-1140.
| Crossref | Google Scholar |

Sitaramam V, Bhate R, Kamalraj P, Pachapurkar S (2008) Respiration hastens maturation and lowers yield in rice. Physiology and Molecular Biology of Plants 14, 253-271.
| Crossref | Google Scholar |

Smitha GR, Thondaiman V (2016) Reproductive biology and breeding system of Saraca asoca (Roxb.) De Wilde: a vulnerable medicinal plant. SpringerPlus 5, 2025.
| Crossref | Google Scholar |

Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology B: Biology 104, 236-257.
| Crossref | Google Scholar | PubMed |

Strasser RJ, Stirbet AD (1998) Heterogeneity of photosystem II probed by the numerically simulated chlorophyll a fluorescence rise (O–J–I–P). Mathematics and Computers in Simulation 48, 3-9.
| 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 Y Mohammad, P Uday, M Prasanna) pp. 445–483. (CRC Press: London, UK) doi:10.1201/9781482268010

Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In ‘Chlorophyll a fluorescence, vol. 19’. Advances in Photosynthesis and Respiration’. (Eds GC Papageorgiou, Govindjee) pp. 321–362. (Springer: Dordrecht, Netherlands) doi:10.1007/978-1-4020-3218-9_12

Swain BB, Mishra S, Mohapatra PK (2023) Fifty years of research on the “bicarbonate effect” in photosystem II: a mini-review. LS – International Journal of Life Sciences 12, 115-140.
| Crossref | Google Scholar |

Tantray AY, Bashir SS, Ahmad A (2020) Low nitrogen stress regulates chlorophyll fluorescence in coordination with photosynthesis and Rubisco efficiency of rice. Physiology and Molecular Biology of Plants 26, 83-94.
| Crossref | Google Scholar |

Uprety DC, Dwivedi N, Raj A, Jaiswal S, Paswan G, Jain V, Maini HK (2009) Study on the response of diploid, tetraploid and hexaploid species of wheat to the elevated CO2. Physiology and Molecular Biology of Plants 15, 161-168.
| Crossref | Google Scholar |

Vogado NO, Cheesman AW, Cernusak LA (2022) Delayed greening during leaf expansion under ambient and elevated CO2 in tropical tree seedlings. Austral Ecology 47, 530-540.
| Crossref | Google Scholar |

Wang C, Gu Q, Zhao L, Li C, Ren J, Zhang J (2022) Photochemical efficiency of photosystem II in inverted leaves of soybean [Glycine max (L.) Merr.] affected by elevated temperature and high light. Frontiers in Plant Science 12, 772644.
| Crossref | Google Scholar |

Wang H, Liu J, Zhao W, Terzaghi W, Deng L, Liu H, Zheng Q, Fan S, Hua W, Zheng M (2023) DELAYED GREENING 409 encodes a dual-localized pentatricopeptide repeat protein required for chloroplast and mitochondrial development. Plant Physiology 192, 2768-2784.
| Crossref | Google Scholar |

Warren CR, Dreyer E (2006) Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. Journal of Experimental Botany 57, 3057-3067.
| Crossref | Google Scholar |

Wong SL, Chen CW, Huang HW, Weng JH (2012) Using combined measurements of gas exchange and chlorophyll fluorescence to investigate the photosynthetic light responses of plant species adapted to different light regimes. Photosynthetica 50, 206-214.
| Crossref | Google Scholar |

Wu B-J, Chow WS, Liu Y-J, Shi L, Jiang C-D (2014) Effects of stomatal development on stomatal conductance and on stomatal limitation of photosynthesis in Syringa oblata and Euonymus japonicus Thunb. Plant Science 229, 23-31.
| Crossref | Google Scholar |

Yang Y-J, Tan S-L, Sun H, Huang J-L, Huang W, Zhang S-B (2021a) Photosystem I is tolerant to fluctuating light under moderate heat stress in two orchids Dendrobium officinale and Bletilla striata. Plant Science 303, 110795.
| Crossref | Google Scholar |

Yang Y-J, Sun H, Zhang S-B, Huang W (2021b) Roles of alternative electron flows in response to excess light in Ginkgo biloba. Plant Science 312, 111030.
| Crossref | Google Scholar |

Yang Y-J, Shi Q, Sun H, Mei R-Q, Huang W (2022) Differential response of the photosynthetic machinery to fluctuating light in mature and young leaves of Dendrobium officinale. Frontiers in Plant Science 12, 829783.
| Crossref | Google Scholar |

Zhang P, Zhang Z, Li B, Zhang H, Hu J, Zhao J (2020) Photosynthetic rate prediction model of newborn leaves verified by core fluorescence parameters. Scientific Reports 10, 3013.
| Crossref | Google Scholar |

Zhang L, Zhang J, Mao Y, Yin Y, Shen X (2022) Physiological analysis and transcriptome sequencing of a delayed-green leaf mutant ‘Duojiao’ of ornamental crabapple (Malus sp.). Physiology and Molecular Biology of Plants 28, 1833-1848.
| Crossref | Google Scholar |

Zhao R, An L, Song D, Li M, Qiao L, Liu N, Sun H (2021) Detection of chlorophyll fluorescence parameters of potato leaves based on continuous wavelet transform and spectral analysis. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 259, 119768.
| Crossref | Google Scholar |

Zhong X, Che X, Zhang Z, Li S, Li Q, Li Y, Gao H (2019) Slower development of PSI activity limits photosynthesis during Euonymus japonicus leaf development. Plant Physiology and Biochemistry 136, 13-21.
| Crossref | Google Scholar |

Zivcak M, Brestic M, Kunderlikova K, Sytar O, Allakhverdiev SI (2015) Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynthesis Research 126, 449-463.
| Crossref | Google Scholar |