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Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum)

Leaves of fullmoon maple (Acer japonicum) turn brilliant red with anthocyanins synthesis in autumn. Based on field observations, autumn coloring mainly occurs in outer-canopy leaves exposed to sun, whereas inner-canopy leaves remain green for a certain longer period before finally turn yellowish red...

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Autores principales: Kitao, Mitsutoshi, Yazaki, Kenichi, Tobita, Hiroyuki, Agathokleous, Evgenios, Kishimoto, Junko, Takabayashi, Atsushi, Tanaka, Ryouichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650427/
https://www.ncbi.nlm.nih.gov/pubmed/36388579
http://dx.doi.org/10.3389/fpls.2022.1006413
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author Kitao, Mitsutoshi
Yazaki, Kenichi
Tobita, Hiroyuki
Agathokleous, Evgenios
Kishimoto, Junko
Takabayashi, Atsushi
Tanaka, Ryouichi
author_facet Kitao, Mitsutoshi
Yazaki, Kenichi
Tobita, Hiroyuki
Agathokleous, Evgenios
Kishimoto, Junko
Takabayashi, Atsushi
Tanaka, Ryouichi
author_sort Kitao, Mitsutoshi
collection PubMed
description Leaves of fullmoon maple (Acer japonicum) turn brilliant red with anthocyanins synthesis in autumn. Based on field observations, autumn coloring mainly occurs in outer-canopy leaves exposed to sun, whereas inner-canopy leaves remain green for a certain longer period before finally turn yellowish red with a smaller amount of anthocyanins. Here, we hypothesized that outer-canopy leaves protect themselves against photooxidative stress via anthocyanins while simultaneously shading inner canopy leaves and protecting them from strong light (holocanopy hypothesis). To test this hypothesis, we investigated photoinhibition and leaf N content during autumn senescence in leaves of pot-grown seedlings of fullmoon maple either raised under shade (L0, ≈13% relative irradiance to open) or transferred to full sunlight conditions on 5(th) (LH1), 12(th) (LH2), or 18(th) (LH3) Oct, 2021. Dry mass-based leaf N (N(mass)) in green leaves in shade-grown seedlings was ≈ 30 mg N g(-1) in summer. N(mass) in shed leaves (25(th) Oct to 1(st) Nov) was 11.1, 12.0, 14.6, and 10.1 mg N g(-1) in L0, LH1, LH2, and LH3 conditions, respectively. Higher N(mass) was observed in shed leaves in LH2, compared to other experimental conditions, suggesting an incomplete N resorption in LH2. F(v)/F(m) after an overnight dark-adaptation, measured on 19(th) Oct when leaf N was actively resorbed, ranked L0: 0.72 > LH3: 0.56 > LH1: 0.45 > LH2: 0.25. As decreased F(v)/F(m) indicates photoinhibition, leaves in LH2 condition suffered the most severe photoinhibition. Leaf soluble sugar content decreased, but protein carbonylation increased with decreasing F(v)/F(m) across shade-grown seedlings (L0, LH1, LH2, and LH3) on 19(th) Oct, suggesting impaired photosynthetic carbon gain and possible membrane peroxidation induced by photooxidative stress, especially in LH2 condition with less N resorption efficiency. Although the impairment of N resorption seems to depend on the timing and intensity of strong light exposure, air temperature, and consequently the degree of photoinhibition, the photoprotective role of anthocyanins in outer-canopy leaves of fullmoon maple might also contribute to allow a safe N resorption in inner-canopy leaves by prolonged shading.
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spelling pubmed-96504272022-11-15 Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum) Kitao, Mitsutoshi Yazaki, Kenichi Tobita, Hiroyuki Agathokleous, Evgenios Kishimoto, Junko Takabayashi, Atsushi Tanaka, Ryouichi Front Plant Sci Plant Science Leaves of fullmoon maple (Acer japonicum) turn brilliant red with anthocyanins synthesis in autumn. Based on field observations, autumn coloring mainly occurs in outer-canopy leaves exposed to sun, whereas inner-canopy leaves remain green for a certain longer period before finally turn yellowish red with a smaller amount of anthocyanins. Here, we hypothesized that outer-canopy leaves protect themselves against photooxidative stress via anthocyanins while simultaneously shading inner canopy leaves and protecting them from strong light (holocanopy hypothesis). To test this hypothesis, we investigated photoinhibition and leaf N content during autumn senescence in leaves of pot-grown seedlings of fullmoon maple either raised under shade (L0, ≈13% relative irradiance to open) or transferred to full sunlight conditions on 5(th) (LH1), 12(th) (LH2), or 18(th) (LH3) Oct, 2021. Dry mass-based leaf N (N(mass)) in green leaves in shade-grown seedlings was ≈ 30 mg N g(-1) in summer. N(mass) in shed leaves (25(th) Oct to 1(st) Nov) was 11.1, 12.0, 14.6, and 10.1 mg N g(-1) in L0, LH1, LH2, and LH3 conditions, respectively. Higher N(mass) was observed in shed leaves in LH2, compared to other experimental conditions, suggesting an incomplete N resorption in LH2. F(v)/F(m) after an overnight dark-adaptation, measured on 19(th) Oct when leaf N was actively resorbed, ranked L0: 0.72 > LH3: 0.56 > LH1: 0.45 > LH2: 0.25. As decreased F(v)/F(m) indicates photoinhibition, leaves in LH2 condition suffered the most severe photoinhibition. Leaf soluble sugar content decreased, but protein carbonylation increased with decreasing F(v)/F(m) across shade-grown seedlings (L0, LH1, LH2, and LH3) on 19(th) Oct, suggesting impaired photosynthetic carbon gain and possible membrane peroxidation induced by photooxidative stress, especially in LH2 condition with less N resorption efficiency. Although the impairment of N resorption seems to depend on the timing and intensity of strong light exposure, air temperature, and consequently the degree of photoinhibition, the photoprotective role of anthocyanins in outer-canopy leaves of fullmoon maple might also contribute to allow a safe N resorption in inner-canopy leaves by prolonged shading. Frontiers Media S.A. 2022-10-28 /pmc/articles/PMC9650427/ /pubmed/36388579 http://dx.doi.org/10.3389/fpls.2022.1006413 Text en Copyright © 2022 Kitao, Yazaki, Tobita, Agathokleous, Kishimoto, Takabayashi and Tanaka https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Kitao, Mitsutoshi
Yazaki, Kenichi
Tobita, Hiroyuki
Agathokleous, Evgenios
Kishimoto, Junko
Takabayashi, Atsushi
Tanaka, Ryouichi
Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum)
title Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum)
title_full Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum)
title_fullStr Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum)
title_full_unstemmed Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum)
title_short Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum)
title_sort exposure to strong irradiance exacerbates photoinhibition and suppresses n resorption during leaf senescence in shade-grown seedlings of fullmoon maple (acer japonicum)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9650427/
https://www.ncbi.nlm.nih.gov/pubmed/36388579
http://dx.doi.org/10.3389/fpls.2022.1006413
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