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Natural variation in the fast phase of chlorophyll a fluorescence induction curve (OJIP) in a global rice minicore panel

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Abstract

Photosynthesis can be probed through Chlorophyll a fluorescence induction (FI), which provides detailed insight into the electron transfer process in Photosystem II, and beyond. Here, we have systematically studied the natural variation of the fast phase of the FI, i.e. the OJIP phase, in rice. The OJIP phase of the Chl a fluorescence induction curve is referred to as “fast transient” lasting for less than a second; it is obtained after a dark-adapted sample is exposed to saturating light. In the OJIP curve, “O” stands for “origin” (minimal fluorescence), “P” for “peak” (maximum fluorescence), and J and I for inflection points between the O and P levels. Further, Fo is the fluorescence intensity at the “O” level, whereas Fm is the intensity at the P level, and Fv (= Fm − Fo) is the variable fluorescence. We surveyed a set of quantitative parameters derived from the FI curves of 199 rice accessions, grown under both field condition (FC) and growth room condition (GC). Our results show a significant variation between Japonica (JAP) and Indica (IND) subgroups, under both the growth conditions, in almost all the parameters derived from the OJIP curves. The ratio of the variable to the maximum (Fv/Fm) and of the variable to the minimum (Fv/Fo) fluorescence, the performance index (PIabs), as well as the amplitude of the I–P phase (AI–P) show higher values in JAP compared to that in the IND subpopulation. In contrast, the amplitude of the O–J phase (AO–J) and the normalized area above the OJIP curve (Sm) show an opposite trend. The performed genetic analysis shows that plants grown under GC appear much more affected by environmental factors than those grown in the field. We further conducted a genome-wide association study (GWAS) using 11 parameters derived from plants grown in the field. In total, 596 non-unique significant loci based on these parameters were identified by GWAS. Several photosynthesis-related proteins were identified to be associated with different OJIP parameters. We found that traits with high correlation are usually associated with similar genomic regions. Specifically, the thermal phase of FI, which includes the amplitudes of the J–I and I–P subphases (AJ–I and AI–P) of the OJIP curve, is, in turn, associated with certain common genomic regions. Our study is the first one dealing with the natural variations in rice, with the aim to characterize potential candidate genes controlling the magnitude and half-time of each of the phases in the OJIP FI curve.

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Abbreviations

βGlu-5:

Oryza sativa 1 β-Glucosidase 5

Chl:

Chlorophyll

FI :

(Chlorophyll a) fluorescence induction

F o :

Basal (initial, minimal) level of chlorophyll a fluorescence

F m :

Maximal level of chlorophyll a fluorescence

F v :

Variable chlorophyll a fluorescence, calculated as Fv = Fm−Fo

FC :

Field condition

GC:

Growth room condition

GWAS:

Genome-wide association study

LED:

Light emitting diode

OJIP transient:

Fast phase of chlorophyll a fluorescence induction, where O is for Fo, P is for peak (equivalent to Fm in saturating light), J and I are for inflections between O and P

RMCP:

Rice minicore panel

QA :

The first quinone electron acceptor of Photosystem II (it is a one-electron acceptor)

QB :

The second quinone electron acceptor of Photosystem II (it is a two-electron acceptor)

PQ:

(Mobile) plastoquinone

PS:

Photosystem

SNP:

Single-nucleotide polymorphism

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Acknowledgements

This work was sponsored by Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDB27020105), National Science Foundation of China (31870214), National Research and Development Program of Ministry of Science and Technology of China (2019YFA0904600; 2019YFA09004600). Govindjee thanks the staff of the Information Technology of Life Sciences, University of Illinois at Urbana-Champaign, for help. We thank members of Prof. Chengcai Chu’s lab for plant growth support for experiments done in Beijing. The study was sponsored by CAS-TWAS President’s Ph.D. Fellowship Program (to Naveed Khan) for international Ph.D. students.

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Authors and Affiliations

  1. CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Institute of Nutrition and Health, University of Chinese Academy of Science, Chinese Academy of Sciences, Shanghai, 200031, China

    Naveed Khan

  2. State Key Laboratory for Plant Molecular Genetics and Center of Excellence for Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, 200031, China

    Naveed Khan, Jemaa Essemine, Saber Hamdani, Mingnan Qu, Ming-Ju Amy Lyu, Shahnaz Perveen & Xin-Guang Zhu

  3. Anne Burras Lane, Newport News, VA, 23606, USA

    Alexandrina Stirbet

  4. Department of Plant Biology, Department of Biochemistry, and Center of Biophysics & Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Govindjee Govindjee

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  1. Naveed Khan
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  2. Jemaa Essemine
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  3. Saber Hamdani
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  4. Mingnan Qu
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  7. Alexandrina Stirbet
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  8. Govindjee Govindjee
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  9. Xin-Guang Zhu
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Contributions

NK, SH, and XZ conceived and conducted the experiments; NK and SH performed most of the experiments, MQ, ML, JE, SP, and XZ provided technical assistance to NK and NK analyzed the data; GG and XZ supervised the experiments; NK wrote most of the text; JE, GG, AS and XZ supervised and complemented the writing of this manuscript.

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Correspondence to Xin-Guang Zhu.

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Since 2019 Govindjee uses Govindjee Govindjee as his legal name.

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Khan, N., Essemine, J., Hamdani, S. et al. Natural variation in the fast phase of chlorophyll a fluorescence induction curve (OJIP) in a global rice minicore panel. Photosynth Res 150, 137–158 (2021). https://doi.org/10.1007/s11120-020-00794-z

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