Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses?

Abstract

Chlorophyll (Chl) a fluorescence induction (transient), measured by exposing dark-adapted samples to high light, shows a polyphasic rise, which has been the subject of extensive research over several decades. Several Chl fluorescence parameters based on this transient have been defined, the most widely used being the FV [= (FM–F0)]/FM ratio as a proxy for the maximum quantum yield of PSII photochemistry. However, considerable additional information may be derived from analysis of the shape of the fluorescence transient. In fact, several performance indices (PIs) have been defined, which are suggested to provide information on the structure and function of PSII, as well as on the efficiencies of specific electron transport reactions in the thylakoid membrane. Further, these PIs have been proposed to quantify plant tolerance to stress, such as by high light, drought, high (or low) temperature, or N-deficiency. This is an interesting idea, since the speed of the Chl a fluorescence transient measurement (<1 s) is very suitable for high-throughput phenotyping. In this review, we describe how PIs have been used in the assessment of photosynthetic tolerance to various abiotic stress factors. We synthesize these findings and draw conclusions on the suitability of several PIs in assessing stress responses. Finally, we highlight an alternative method to extract information from fluorescence transients, the Integrated Biomarker Response. This method has been developed to define multi-parametric indices in other scientific fields (e.g., ecology), and may be used to combine Chl a fluorescence data with other proxies characterizing CO2 assimilation, or even growth or grain yield, allowing a more holistic assessment of plant performance.

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Abbreviations

ABS:

photon flux absorbed by the antenna of PSII units

Area:

area above the OJIP transient

CFI:

chill factor index

Chl:

chlorophyll

CS:

cross section

Cyt:

cytochrome

DF:

driving force

DFI:

drought factor index

DI:

flux of energy dissipation (through processes other than trapping) in the antenna of PSII units

ET:

rate of electron transport from the reduced QA to the intersystem electron acceptors

F0 :

minimum Chl a fluorescence

Fd:

ferredoxin

FI:

fluorescence induction

FM :

maximum Chl a fluorescence

FT :

terminal steady state of Chl a fluorescence

HSI:

heat sensitivity index

I step:

Chl a fluorescence at ~ 30 ms

IBR:

integrated biomarker response

J step:

Chl a fluorescence at ~ 2 ms

K step:

Chl a fluorescence at ~ 0.3 ms

M0 :

initial slope (first 0.3 ms) of the O-J fluorescence rise

NPQ:

nonphotochemical quenching of the excited states of Chl

OEC:

oxygen-evolving complex

P680:

reaction center Chls of PSII

PC:

plastocyanin

Phe:

pheophytin

PSi:

photochemical stress index

PI:

performance index

PILR:

performance index leaf ratio

PQ:

plastoquinone

RE:

rate of electron transport from the reduced QA to the final electron acceptors of PSI

Rfd :

ratio of fluorescence decrease to steady state fluorescence

ROS:

reactive oxygen species

RWC:

relative water content

SFI:

structure-function index

Sm :

normalized area above the OJIP transient

TR:

flux of exciton trapping by active PSII reaction centers leading to QA reduction

ΔVIP :

relative amplitude of the I–P phase of Chl a fluorescence

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Three of the authors (Alexandrina Stirbet, Dušan Lazár and Johannes Kromdijk) pay tribute to their coauthor (Govindjee) for his lifetime work, at his 85thbirthday (on October 24, 2017). They write: “Besides his many achievements, Govindjee is well known in the photosynthesis research community for his passion and excitement in relating chlorophyll (Chl) a fluorescence to photosynthesis; this started with his discovery, in 1960, of the two-light effect on Chl a fluorescence, and it continues till today.” Stirbet wrote: “I met Govindjee in 1995 in Geneva, Switzerland, when he was visiting Reto Strasser’s lab, and we wrote a paper on modeling the Chl a fluorescence transient, the OJIP phase (Stirbet et al. 1998). In 2010, we restarted our collaboration, and published several reviews, as well as experimental and theoretical papers, still on Chl fluorescence, and I am looking forward to continue our work together”. Lazár added: “My first contact with Govindjee dates back to the final stages of my Ph.D. studies, when I submitted a review paper to Biochimica et Biophysica Acta on Chl fluorescence induction (Lazár 1999), and Govindjee was one of its reviewers; he had declared his identity. From that time, I know Govindjee as a bright, accurate and enthusiastic scientist, who also supports (and encourages) alternate views [see e.g., my theoretical paper (Lazár 2013) on variable Chl fluorescence originating in PSI, which he had also reviewed].” Kromdijk added: “Doing photosynthesis-related research on the Urbana-Champaign Campus of the University of Illinois (USA), it is impossible not to cross paths with Govindjee. I met Govindjee a few years ago after relocating to Urbana-Champaign for my postdoctoral research. Since then, we regularly meet up to drink coffee and talk about life and anything related to photosynthesis. Govindjee has an incredible lifetime of photosynthetic research and experiences to share, and combines this with the passion and enthusiasm of someone who just discovered the topic yesterday.”

Acknowledgement: D.L. was supported by a grant # LO1204 (Sustainable Development of Research in the Centre of the Region Haná) from the National Program of Sustainability I, Ministry of Education, Youth and Sports, Czech Republic. J.K. was supported by the Bill and Melinda Gates Foundation (grant OPP1060461). Govindjee was supported by the Department of Plant Biology (James Dalling, Head), and the Department of Biochemistry (Susan Martinis, Head) of the University of Illinois at Urbana-Champaign, IL, USA.

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Stirbet, A., Lazár, D., Kromdijk, J. et al. Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses?. Photosynthetica 56, 86–104 (2018). https://doi.org/10.1007/s11099-018-0770-3

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Additional key words

  • JIP-test
  • Kautsky effect
  • performance index
  • tolerance to stress