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Cited by 33Photosynthetic Processes and MechanismsPlant Stress Responses and ToleranceLight effects on plants

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Differential Mechanisms of Photosynthetic Acclimation to Light and Low Temperature in Arabidopsis and the Extremophile Eutrema salsugineum

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Khanal, Nityananda, Bray, Geoffrey, Grisnich, Anna, Moffatt, Barbara, Gray, Gordon·2017·Plants
DOI 10.3390/plants6030032PMC PMC5620588
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Abstract

Photosynthetic organisms are able to sense energy imbalances brought about by the overexcitation of photosystem II (PSII) through the redox state of the photosynthetic electron transport chain, estimated as the chlorophyll fluorescence parameter 1-qL, also known as PSII excitation pressure. Plants employ a wide array of photoprotective processes that modulate photosynthesis to correct these energy imbalances. Low temperature and light are well established in their ability to modulate PSII excitation pressure. The acquisition of freezing tolerance requires growth and development a low temperature (cold acclimation) which predisposes the plant to photoinhibition. Thus, photosynthetic acclimation is essential for proper energy balancing during the cold acclimation process. Eutrema salsugineum (Thellungiella salsuginea) is an extremophile, a close relative of Arabidopsis thaliana, but possessing much higher constitutive levels of tolerance to abiotic stress. This comparative study aimed to characterize the photosynthetic properties of Arabidopsis (Columbia accession) and two accessions of Eutrema (Yukon and Shandong) isolated from contrasting geographical locations at cold acclimating and non-acclimating conditions. In addition, three different growth regimes were utilized that varied in temperature, photoperiod and irradiance which resulted in different levels of PSII excitation pressure. This study has shown that these accessions interact differentially to instantaneous (measuring) and long-term (acclimation) changes in PSII excitation pressure with regard to their photosynthetic behaviour. Eutrema accessions contained a higher amount of photosynthetic pigments, showed higher oxidation of P700 and possessed more resilient photoprotective mechanisms than that of Arabidopsis, perhaps through the prevention of PSI acceptor-limitation. Upon comparison of the two Eutrema accessions, Shandong demonstrated the greatest PSII operating efficiency (ΦPSII) and P700 oxidizing capacity, while Yukon showed greater growth plasticity to irradiance. Both of these Eutrema accessions are able to photosynthetically acclimate but do so by different mechanisms. The Shandong accessions demonstrate a stable response, favouring energy partitioning to photochemistry while the Yukon accession shows a more rapid response with partitioning to other (non-photochemical) strategies.

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Figure 1 Maximum quantum efficiency of PSII (Fv/Fm) of non-acclimated and cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). PSII = photosystem II; SE = standard error. Means were grouped by Fisher’s individual error rate at significance level of 0.05.
Figure 1 Maximum quantum efficiency of PSII (Fv/Fm) of non-acclimated and cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). PSII = photosystem II; SE = standard error. Means were grouped by Fisher’s individual error rate at significance level of 0.05.CC BY · PubMed Central
Figure 2 Photoinhibition and recovery measured as changes in maximum quantum efficiency of PSII (Fv/Fm) for (A) non-acclimated and (B) cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). Photoinhibition occurred for 4 h with a photosynthetic photon flux density (PPFD) of 1750 μmol photons m−2 s−1 at 7 °C. Recovery occurred at 22 °C under dim light (30 μmol photons m−2 s−1) for 24 h. Values represent means ± SE (n = 3 to 6). PSII = photosystem II; SE = standard error. Fisher’s individual error rate at significance level of 0.05 was used for inter-specific means comparison.
Figure 2 Photoinhibition and recovery measured as changes in maximum quantum efficiency of PSII (Fv/Fm) for (A) non-acclimated and (B) cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). Photoinhibition occurred for 4 h with a photosynthetic photon flux density (PPFD) of 1750 μmol photons m−2 s−1 at 7 °C. Recovery occurred at 22 °C under dim light (30 μmol photons m−2 s−1) for 24 h. Values represent means ± SE (n = 3 to 6). PSII = photosystem II; SE = standard error. Fisher’s individual error rate at significance level of 0.05 was used for inter-specific means comparison.CC BY · PubMed Central
Figure 3 Light response curves of 1-qL for Eutrema accessions and Arabidopsis developed under three different growth regimes. Non-acclimated and cold acclimated plants of Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were subjected to their respective growth temperatures (A–C) as well as reciprocal temperature measurements (D–F). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). CACM = cold acclimated cold-measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; PSII = photosystem II; 1-qL = PSII excitation pressure; SE = standard error.
Figure 3 Light response curves of 1-qL for Eutrema accessions and Arabidopsis developed under three different growth regimes. Non-acclimated and cold acclimated plants of Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were subjected to their respective growth temperatures (A–C) as well as reciprocal temperature measurements (D–F). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). CACM = cold acclimated cold-measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; PSII = photosystem II; 1-qL = PSII excitation pressure; SE = standard error.CC BY · PubMed Central
Figure 4 Light response curves of RETRPSII for Eutrema accessions and Arabidopsis developed under three different growth regimes. Non-acclimated and cold acclimated plants of Yukon (Yu), Shandong (Sh) and Arabidopsis (At) subjected to their respective growth temperatures (A–C) as well as reciprocal temperature measurements (D–F). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; RETRPSII, non-cyclic electron transport rate through PSII; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; PSII = photosystem II; SE = standard error.
Figure 4 Light response curves of RETRPSII for Eutrema accessions and Arabidopsis developed under three different growth regimes. Non-acclimated and cold acclimated plants of Yukon (Yu), Shandong (Sh) and Arabidopsis (At) subjected to their respective growth temperatures (A–C) as well as reciprocal temperature measurements (D–F). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; RETRPSII, non-cyclic electron transport rate through PSII; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; PSII = photosystem II; SE = standard error.CC BY · PubMed Central
Figure 5 Light response curves of qO for Eutrema accessions and Arabidopsis developed under three different growth regimes. Non-acclimated and cold acclimated plants of Yukon (Yu), Shandong (Sh) and Arabidopsis (At) subjected to their respective growth temperatures (A–C) as well as reciprocal temperature measurements (D–F). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; qO = coefficient of basal fluorescence quenching; SE = standard error.
Figure 5 Light response curves of qO for Eutrema accessions and Arabidopsis developed under three different growth regimes. Non-acclimated and cold acclimated plants of Yukon (Yu), Shandong (Sh) and Arabidopsis (At) subjected to their respective growth temperatures (A–C) as well as reciprocal temperature measurements (D–F). No results were obtained for the Yukon accession in the non-acclimated Arabidopsis regime due to poor growth. Values represent means ± SE (n = 3 to 6). CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; qO = coefficient of basal fluorescence quenching; SE = standard error.CC BY · PubMed Central
Figure 6 Partitioning of excitation energy as a function of irradiance for Eutrema accessions and Arabidopsis. The fraction of excitation energy flow via PSII photochemistry (ΦPSII) and non-photochemical dissipation pathways (ΦNO and ΦNPQ) in Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were estimated for plants developed under a Yukon growth regime. Non-acclimated and cold acclimated plants were subjected to their respective growth temperatures as well as reciprocal temperature measurements. CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; NPQ = non-photochemical quenching; PSII = photosystem II; ΦNO = efficiency of constitutive non-photochemical energy dissipation and fluorescence; ΦNPQ = efficiency of light dependent NPQ; ΦPSII = PSII operating efficiency.
Figure 6 Partitioning of excitation energy as a function of irradiance for Eutrema accessions and Arabidopsis. The fraction of excitation energy flow via PSII photochemistry (ΦPSII) and non-photochemical dissipation pathways (ΦNO and ΦNPQ) in Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were estimated for plants developed under a Yukon growth regime. Non-acclimated and cold acclimated plants were subjected to their respective growth temperatures as well as reciprocal temperature measurements. CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; NPQ = non-photochemical quenching; PSII = photosystem II; ΦNO = efficiency of constitutive non-photochemical energy dissipation and fluorescence; ΦNPQ = efficiency of light dependent NPQ; ΦPSII = PSII operating efficiency.CC BY · PubMed Central
Figure 7 Partitioning of excitation energy as a function of irradiance for Eutrema accessions and Arabidopsis. The fraction of excitation energy flow via PSII photochemistry (ΦPSII) and non-photochemical dissipation pathways (ΦNO and ΦNPQ) in Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were estimated for plants developed under a Shandong growth regime. Non-acclimated and cold acclimated plants were subjected to their respective growth temperatures as well as reciprocal temperature measurements. CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; NPQ = non-photochemical quenching; PSII = photosystem II; ΦNO = efficiency of constitutive non-photochemical energy dissipation and fluorescence; ΦNPQ = efficiency of light dependent NPQ; ΦPSII = PSII operating efficiency.
Figure 7 Partitioning of excitation energy as a function of irradiance for Eutrema accessions and Arabidopsis. The fraction of excitation energy flow via PSII photochemistry (ΦPSII) and non-photochemical dissipation pathways (ΦNO and ΦNPQ) in Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were estimated for plants developed under a Shandong growth regime. Non-acclimated and cold acclimated plants were subjected to their respective growth temperatures as well as reciprocal temperature measurements. CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; NPQ = non-photochemical quenching; PSII = photosystem II; ΦNO = efficiency of constitutive non-photochemical energy dissipation and fluorescence; ΦNPQ = efficiency of light dependent NPQ; ΦPSII = PSII operating efficiency.CC BY · PubMed Central
Figure 8 Partitioning of excitation energy as a function of irradiance for Eutrema accessions and Arabidopsis. The fraction of excitation energy flow via PSII photochemistry (ΦPSII) and non-photochemical dissipation pathways (ΦNO and ΦNPQ) in Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were estimated for plants developed under an Arabidopsis growth regime. Non-acclimated and cold acclimated plants were subjected to their respective growth temperatures as well as reciprocal temperature measurements. The blank graphs of the Yukon accession denote no results obtained due to poor growth of the accession in that condition. CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; NPQ = non-photochemical quenching; PSII = photosystem II; ΦNO = efficiency of constitutive non-photochemical energy dissipation and fluorescence; ΦNPQ = efficiency of light dependent NPQ; ΦPSII = PSII operating efficiency.
Figure 8 Partitioning of excitation energy as a function of irradiance for Eutrema accessions and Arabidopsis. The fraction of excitation energy flow via PSII photochemistry (ΦPSII) and non-photochemical dissipation pathways (ΦNO and ΦNPQ) in Yukon (Yu), Shandong (Sh) and Arabidopsis (At) were estimated for plants developed under an Arabidopsis growth regime. Non-acclimated and cold acclimated plants were subjected to their respective growth temperatures as well as reciprocal temperature measurements. The blank graphs of the Yukon accession denote no results obtained due to poor growth of the accession in that condition. CACM = cold acclimated cold measured; CAWM = cold acclimated warm-measured; NACM = non-acclimated cold measured; NAWM = non-acclimated warm-measured; NPQ = non-photochemical quenching; PSII = photosystem II; ΦNO = efficiency of constitutive non-photochemical energy dissipation and fluorescence; ΦNPQ = efficiency of light dependent NPQ; ΦPSII = PSII operating efficiency.CC BY · PubMed Central
Figure 9 P700 oxidation measured as ΔA820 for (A) non-acclimated and (B) cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). Plants were measured at room (20 °C) and cold (4.5 °C) temperatures. Values represent means ± SE (n = 4 to 9). SE = standard error.
Figure 9 P700 oxidation measured as ΔA820 for (A) non-acclimated and (B) cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). Plants were measured at room (20 °C) and cold (4.5 °C) temperatures. Values represent means ± SE (n = 4 to 9). SE = standard error.CC BY · PubMed Central
Figure 10 Pool size of electrons in the intersystem chain (e−/P700) for (A) non-acclimated and (B) cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). Plants were measured at room (20 °C) and cold (4.5 °C) temperatures. Values represent means ± SE (n = 4 to 9). SE = standard error.
Figure 10 Pool size of electrons in the intersystem chain (e−/P700) for (A) non-acclimated and (B) cold acclimated Eutrema accessions and Arabidopsis developed under three different growth regimes. Yukon accession (■); Shandong accession (■); Arabidopsis (■). Plants were measured at room (20 °C) and cold (4.5 °C) temperatures. Values represent means ± SE (n = 4 to 9). SE = standard error.CC BY · PubMed Central

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Metadata

Authors
Khanal, N., Bray, G., Grisnich, A., Moffatt, B., & Gray, G.
Affiliations
  • University of Saskatchewan (CA)
  • University of Waterloo (CA)
Corresponding author
Gray, Gordon
ORCID
Khanal, Nityananda
Venue
Plants
Publisher
MDPI AG
Published
2017-08-09
Volume
6
Issue
3
Pages
32
ISSN
2223-7747 (ISSN-L)
DOI
10.3390/plants6030032
PMC
PMC5620588
OpenAlex
W2742831901
Cited by
32
References
67
Citations by year
2025: 3 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 11 · 2019: 2 · 2018: 2
FWCI
1.68
Type
journal article
Language
en
Open access
Licence
Locations
  • Plants (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Federal Open Science Repository of Canada / Le Dépôt fédéral de science ouverte du Canada (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Natural Sciences and Engineering Research Council of Canada
  • Agriculture and Agri-Food Canada
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
Keywords
photosynthetic acclimation, cold acclimation, photoprotection, Eutrema salsugineum, Thellungiella salsuginea, Arabidopsis thaliana, freezing tolerance, photoinhibition, P700 oxidation, photosynthetic pigments, non-photochemical quenching, energy allocation, photoperiod, irradiance, extremophile plants

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