Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Disentangling the photosynthesis performance in japonica rice during natural leaf senescence using OJIP fluorescence transient analysis

Faliang Zeng A , Guojiao Wang A B , Yinpei Liang A , Naihui Guo A , Lin Zhu A , Qi Wang A , Hongwei Chen A , Dianrong Ma A and Jiayu Wang https://orcid.org/0000-0001-7967-0725 A B
+ Author Affiliations
- Author Affiliations

A Rice Research Institute, Shenyang Agricultural University, Shenyang, 110866, China.

B Corresponding authors. Email: syaurice@syau.edu.cn; wangjiayu@syau.edu.cn

Functional Plant Biology 48(2) 206-217 https://doi.org/10.1071/FP20104
Submitted: 9 April 2020  Accepted: 18 September 2020   Published: 26 October 2020

Abstract

Rice undergoes leaf senescence accompanied with grain filling when the plants reach the end of their temporal niche, and a delay in leaf senescence ultimately improves the yield and quality of grain. To estimate the decline in photosynthesis during leaf senescence and to find an efficient and useful tool to identify rice genotypes with a longer duration of active photosynthesis, we examined PSII photosynthetic activity in the flag leaves of japonica rice Shennong265 (SN265) and Beigeng3 (BG3) during leaf senescence using chlorophyll a fluorescence kinetics. The results show that inhibition occurred in the electron transport chains, but the energetic connectivity of PSII units was not affected as dramatically during leaf senescence. PSII reaction centres (RCs) were transformed into ‘silent RCs,’ and the chlorophyll content decreased during leaf senescence. However the size of the ‘economic’ antennae increased. Further, the percentage of variation of the specific energy flux parameters can rationally be used to indicate leaf senescence from the perspective of energy balance. Although the performance indices were more sensitive than other functional and structural JIP-test parameters, they still did not serve as an indicator of crop yield.

Keywords: chlorophyll fluorescence, grain filling, JIP-test, leaf senescence, Oryza sativa, photosynthesis, PSII, yield.


References

Abeles FB, Dunn LJ, Morgens P, Callahan A, Dinterman RE, Schmidt J (1988) Induction of 33-kD and 60-kD peroxidases during ethylene-induced senescence of cucumber cotyledons. Plant Physiology 87, 609–615.
Induction of 33-kD and 60-kD peroxidases during ethylene-induced senescence of cucumber cotyledons.Crossref | GoogleScholarGoogle Scholar | 16666194PubMed |

Ambavaram MMR, Basu S, Krishnan A, Ramegowda V, Batlang U, Rahman L, Baisakh N, Pereira A (2014) Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress. Nature Communications 5, 5302
Coordinated regulation of photosynthesis in rice increases yield and tolerance to environmental stress.Crossref | GoogleScholarGoogle Scholar |

Avila-Ospina L, Moison M, Yoshimoto K, Masclaux-Daubresse C (2014) Autophagy, plant senescence, and nutrient recycling. Journal of Experimental Botany 65, 3799–3811.
Autophagy, plant senescence, and nutrient recycling.Crossref | GoogleScholarGoogle Scholar | 24687977PubMed |

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.
Leaf and plant age affects photosynthetic performance and photoprotective capacity.Crossref | GoogleScholarGoogle Scholar | 29018097PubMed |

Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiology 59, 411–416.
Involvement of hydrogen peroxide in the regulation of senescence in pear.Crossref | GoogleScholarGoogle Scholar | 16659863PubMed |

Chen S, Yang J, Zhang M, Strasser RJ, Qiang S (2016) Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P. Environmental and Experimental Botany 122, 126–140.
Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P.Crossref | GoogleScholarGoogle Scholar |

Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochimica et Biophysica Acta – Bioenergetics 1847, 468–485.
Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change.Crossref | GoogleScholarGoogle Scholar |

Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Analytical Biochemistry 70, 616–620.
Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase.Crossref | GoogleScholarGoogle Scholar | 817618PubMed |

Fitzgerald MA, McCouch SR, Hall RD (2009) Not just a grain of rice: the quest for quality. Trends in Plant Science 14, 133–139.
Not just a grain of rice: the quest for quality.Crossref | GoogleScholarGoogle Scholar | 19230745PubMed |

Grassini P, Eskridge KM, Cassman KG (2013) Distinguishing between yield advances and yield plateaus in historical crop production trends. Nature Communications 4, 2918
Distinguishing between yield advances and yield plateaus in historical crop production trends.Crossref | GoogleScholarGoogle Scholar | 24346131PubMed |

Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biology 10, 37–49.
Leaf senescence and nutrient remobilisation in barley and wheat.Crossref | GoogleScholarGoogle Scholar | 18721310PubMed |

Gregersen PL, Culetic A, Boschian L, Krupinska K (2013) Plant senescence and crop productivity. Plant Molecular Biology 82, 603–622.
Plant senescence and crop productivity.Crossref | GoogleScholarGoogle Scholar | 23354836PubMed |

Gu J, Zhou Z, Li Z, Chen Y, Wang Z, Zhang H, Yang J (2017) Photosynthetic properties and potentials for improvement of photosynthesis in pale green leaf rice under high light conditions. Frontiers in Plant Science 8, 1082
Photosynthetic properties and potentials for improvement of photosynthesis in pale green leaf rice under high light conditions.Crossref | GoogleScholarGoogle Scholar | 28676818PubMed |

Gururani MA, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Molecular Plant 8, 1304–1320.
Regulation of photosynthesis during abiotic stress-induced photoinhibition.Crossref | GoogleScholarGoogle Scholar | 25997389PubMed |

Holland V, Koller S, Brüggemann W (2014) Insight into the photosynthetic apparatus in evergreen and deciduous European oaks during autumn senescence using OJIP fluorescence transient analysis. Plant Biology 16, 801–808.
Insight into the photosynthetic apparatus in evergreen and deciduous European oaks during autumn senescence using OJIP fluorescence transient analysis.Crossref | GoogleScholarGoogle Scholar | 24112772PubMed |

Holland V, Fragner L, Jungcurt T, Weckwerth W, Brüggemann W (2016) Girdling interruption between source and sink in Quercus pubescens does not trigger leaf senescence. Photosynthetica 54, 589–597.
Girdling interruption between source and sink in Quercus pubescens does not trigger leaf senescence.Crossref | GoogleScholarGoogle Scholar |

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.
Improving photosynthesis and crop productivity by accelerating recovery from photoprotection.Crossref | GoogleScholarGoogle Scholar | 27856901PubMed |

Li XM, Chen MJ, Li J, Ma LJ, Bu N, Li YY, Zhang LH (2014) Effect of endophyte infection on chlorophyll a fluorescence in salinity stressed rice. Biologia Plantarum 58, 589–594.
Effect of endophyte infection on chlorophyll a fluorescence in salinity stressed rice.Crossref | GoogleScholarGoogle Scholar |

Lim PO, Kim HJ, Gil Nam H (2007) Leaf senescence. Annual Review of Plant Biology 58, 115–136.
Leaf senescence.Crossref | GoogleScholarGoogle Scholar | 17177638PubMed |

Luo H, Merope T, Zhang Y, Zhang W (2016) Combining gas exchange and chlorophyll a fluorescence measurements to analyze the photosynthetic activity of drip-irrigated cotton under different soil water deficits. Journal of Integrative Agriculture 15, 1256–1266.
Combining gas exchange and chlorophyll a fluorescence measurements to analyze the photosynthetic activity of drip-irrigated cotton under different soil water deficits.Crossref | GoogleScholarGoogle Scholar |

Maehly AC, Chance B (1954) The assay of catalases and peroxidases. In ‘Methods of biochemical analysis. Vol. 1’. (Ed. D Glick) pp. 357–424. (Interscience Publishers: New York)

Masclaux C, Valadier MH, Brugière N, Hirel MG (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211, 510–518.
Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence.Crossref | GoogleScholarGoogle Scholar | 11030550PubMed |

Mereu S, Gerosa G, Marzuoli R, Fusaro L, Salvatori E, Finco A, Spanoa D, Manes F (2011) Gas exchange and JIP-test parameters of two Mediterranean maquis species are affected by sea spray and ozone interaction. Environmental and Experimental Botany 73, 80–88.
Gas exchange and JIP-test parameters of two Mediterranean maquis species are affected by sea spray and ozone interaction.Crossref | GoogleScholarGoogle Scholar |

Miersch I, Heise J, Zelmer I, Humbeck K (2000) Differential degradation of the photosynthetic apparatus during leaf senescence in barley (Hordeum vulgare L.). Plant Biology 2, 618–623.
Differential degradation of the photosynthetic apparatus during leaf senescence in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar |

Nicol L, Nawrocki WJ, Croce R (2019) Disentangling the sites of non-photochemical quenching in vascular plants. Nature Plants 5, 1177–1183.
Disentangling the sites of non-photochemical quenching in vascular plants.Crossref | GoogleScholarGoogle Scholar | 31659240PubMed |

Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynthesis Research 84, 1–7.

Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta – Bioenergetics 1757, 742–749.
A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II.Crossref | GoogleScholarGoogle Scholar |

Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiologia Plantarum 142, 35–46.

Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Long SP, Moore TA, Moroney J, Niyogi KK, Parry MAJ, Peralta-Yahya PP, Prince RC, Redding KE, Spalding MH, Wijky KJV, Vermaas WFJ, Caemmereraa SV, Weber APM, Yeates TO, Yuan JS, Zhu XG (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proceedings of the National Academy of Sciences of the United States of America 112, 8529–8536.

Osmond B, Chow WS, Wyber R, Zavafer A, Keller B, Pogson BJ, Robinson SA (2017) Relative functional and optical absorption cross-sections of PSII and other photosynthetic parameters monitored in situ, at a distance with a time resolution of a few seconds, using a prototype light induced fluorescence transient (LIFT) device. Functional Plant Biology 44, 985–1006.
Relative functional and optical absorption cross-sections of PSII and other photosynthetic parameters monitored in situ, at a distance with a time resolution of a few seconds, using a prototype light induced fluorescence transient (LIFT) device.Crossref | GoogleScholarGoogle Scholar | 32480627PubMed |

Osmond B, Chow WS, Pogson BJ, Robinson SA (2019) Probing functional and optical cross-sections of PSII in leaves during state transitions using fast repetition rate light induced fluorescence transients. Functional Plant Biology 46, 567–583.
Probing functional and optical cross-sections of PSII in leaves during state transitions using fast repetition rate light induced fluorescence transients.Crossref | GoogleScholarGoogle Scholar | 32172734PubMed |

Papanatsiou M, Petersen J, Henderson L, Wang Y, Christie JM, Blatt MR (2019) Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth. Science 363, 1456–1459.
Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth.Crossref | GoogleScholarGoogle Scholar | 30923223PubMed |

Perbonip AT, Martinnazzo EG, Moura AB, Bacarin MA (2019) Can be performance indexes used to select plant growth-promoting rhizobacteria? Photosynthetica 57, 68–76.

Qian Q, Guo L, Smith SM, Li J (2016) Breeding high-yield superior-quality hybrid super-rice by rational design. National Science Review 3, 283–294.
Breeding high-yield superior-quality hybrid super-rice by rational design.Crossref | GoogleScholarGoogle Scholar |

Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS One 8, e66428
Yield trends are insufficient to double global crop production by 2050.Crossref | GoogleScholarGoogle Scholar | 23840465PubMed |

Redillas MCFR, Jeong JS, Strasser RJ, Kim YS, Kim JK (2011a) JIP analysis on rice (Oryza sativa cv Nipponbare) grown under limited nitrogen conditions. Journal of the Korean Society for Applied Biological Chemistry 54, 827–832.
JIP analysis on rice (Oryza sativa cv Nipponbare) grown under limited nitrogen conditions.Crossref | GoogleScholarGoogle Scholar |

Redillas MCFR, Strasser RJ, Jeong JS, Kim YS, Kim JK (2011b) The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing osnac10. Plant Biotechnology Reports 5, 169–175.
The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing osnac10.Crossref | GoogleScholarGoogle Scholar |

Sarkar RK, Panda D (2009) Distinction and characterisation of submergence tolerant and sensitive rice cultivars, probed by the fluorescence OJIP rise kinetics. Functional Plant Biology 36, 222–233.
Distinction and characterisation of submergence tolerant and sensitive rice cultivars, probed by the fluorescence OJIP rise kinetics.Crossref | GoogleScholarGoogle Scholar | 32688641PubMed |

Sarkar RK, Ray A (2016) Submergence-tolerant rice withstands complete submergence even in saline water: probing through chlorophyll a fluorescence induction O-J-J-P transients. Photosynthetica 54, 275–287.
Submergence-tolerant rice withstands complete submergence even in saline water: probing through chlorophyll a fluorescence induction O-J-J-P transients.Crossref | GoogleScholarGoogle Scholar |

Sartory DP, Grobbelaar JU (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 114, 177–187.
Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis.Crossref | GoogleScholarGoogle Scholar |

Sitko K, Rusinowski S, Pogrzeba M, Daszkowska-Golec A, Gieroń Ż, Kalaji HM, Małkowski E (2020) Development and aging of photosynthetic apparatus of Vitis vinifera L. during growing season. Photosynthetica 58, 186–193.
Development and aging of photosynthetic apparatus of Vitis vinifera L. during growing season.Crossref | GoogleScholarGoogle Scholar |

South PF, Cavanagh AP, Liu HW, Ort DR (2019) Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363, eaat9077
Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field.Crossref | GoogleScholarGoogle Scholar | 30606819PubMed |

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.
On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient.Crossref | GoogleScholarGoogle Scholar | 21295993PubMed |

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 & Francis: London)

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

Strasserf RJ, Srivastava A (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology 61, 32–42.
Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

Tsimilli-Michael M (2019) Revisiting JIP-test: an educative review on concepts, assumptions, approximations, definitions and terminology. Photosynthetica 57, 90–107.

von Caemmerer SV, Quick WP, Furbank RT (2012) The development of C4 rice: current progress and future challenges. Science 336, 1671–1672.
The development of C4 rice: current progress and future challenges.Crossref | GoogleScholarGoogle Scholar |

Wang LJ, Fan L, Loescher W, Duan W, Liu GJ, Cheng JS, Luo HB, Li SH (2010) Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biology 10, 34
Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves.Crossref | GoogleScholarGoogle Scholar | 20178597PubMed |

Wang Y, Zhang J, Yu J, Jiang X, Sun L, Wu M, Chen G, Lv C (2014) Photosynthetic changes of flag leaves during senescence stage in super high-yield hybrid rice LYPJ grown in field condition. Plant Physiology and Biochemistry 82, 194–201.
Photosynthetic changes of flag leaves during senescence stage in super high-yield hybrid rice LYPJ grown in field condition.Crossref | GoogleScholarGoogle Scholar | 24976603PubMed |

Wang YW, Xu C, Lv CF, Wu M, Cai XJ, Liu ZT, Song XM, Chen GX, Lv CG (2016) Chlorophyll a fluorescence analysis of high-yield rice (Oryza sativa L.) LYPJ during leaf senescence. Photosynthetica 54, 422–429.
Chlorophyll a fluorescence analysis of high-yield rice (Oryza sativa L.) LYPJ during leaf senescence.Crossref | GoogleScholarGoogle Scholar |

Woo HR, Chung KM, Park JH, Oh SA, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-Box protein that regulates leaf senescence in Arabidopsis. The Plant Cell 13, 1779–1790.
ORE9, an F-Box protein that regulates leaf senescence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11487692PubMed |

Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee , Sarin NB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochimica et Biophysica Acta – Bioenergetics 1797, 1428–1438.
Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements.Crossref | GoogleScholarGoogle Scholar |

Zhang M, Shan YJ, Kochian L, Strasser RJ, Chen GX (2015) Photochemical properties in flag leaves of a super-high-yielding hybrid rice and a traditional hybrid rice (Oryza sativa L.) probed by chlorophyll a fluorescence transient. Photosynthesis Research 126, 275–284.
Photochemical properties in flag leaves of a super-high-yielding hybrid rice and a traditional hybrid rice (Oryza sativa L.) probed by chlorophyll a fluorescence transient.Crossref | GoogleScholarGoogle Scholar | 25972274PubMed |

Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annual Review of Plant Biology 61, 235–261.
Improving photosynthetic efficiency for greater yield.Crossref | GoogleScholarGoogle Scholar | 20192734PubMed |

Zubek S, Turnau K, Tsimilli-Michael M, Strasser RJ (2009) Response of endangered plant species to inoculation with arbuscular mycorrhizal fungi and soil bacteria. Mycorrhiza 19, 113–123.
Response of endangered plant species to inoculation with arbuscular mycorrhizal fungi and soil bacteria.Crossref | GoogleScholarGoogle Scholar | 19011910PubMed |