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

Both external and internal factors induce heterogeneity in senescing leaves of deciduous trees

Heta Mattila https://orcid.org/0000-0002-5071-9721 A B * , Sergey Khorobrykh https://orcid.org/0000-0002-0153-5133 A and Esa Tyystjärvi https://orcid.org/0000-0001-6808-7470 A
+ Author Affiliations
- Author Affiliations

A Molecular Plant Biology, University of Turku, Turku, Finland.

B Centre for Environmental and Marine Studies, University of Aveiro, Aveiro, Portugal.

* Correspondence to: h.mattila@ua.pt

Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 51, FP24012 https://doi.org/10.1071/FP24012
Submitted: 9 January 2024  Accepted: 23 March 2024  Published: 15 April 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Autumn senescence is characterised by spatial and temporal heterogeneity. We show that senescing birch (Betula spp.) leaves had lower PSII activity (probed by the FV/FM chlorophyll a fluorescence parameter) in late autumn than in early autumn. We confirmed that PSII repair slows down with decreasing temperature, while rates of photodamage and recovery, measured under laboratory conditions at 20°C, were similar in these leaves. We propose that low temperatures during late autumn hinder repair and lead to accumulation of non-functional PSII units in senescing leaves. Fluorescence imaging of birch revealed that chlorophyll preferentially disappeared from inter-veinal leaf areas. These areas showed no recovery capacity and low non-photochemical quenching while green veinal areas of senescing leaves resembled green leaves. However, green and yellow leaf areas showed similar values of photochemical quenching. Analyses of thylakoids isolated from maple (Acer platanoides) leaves showed that red, senescing leaves contained high amounts of carotenoids and α-tocopherol, and our calculations suggest that α-tocopherol was synthesised during autumn. Thylakoids isolated from red maple leaves produced little singlet oxygen, probably due to the high antioxidant content. However, the rate of PSII photodamage did not decrease. The data show that the heterogeneity of senescing leaves must be taken into account to fully understand autumn senescence.

Keywords: Acer platanoides, anthocyanin, autumnal, Betula pendula, Betula pubescens, photoinhibition, reactive oxygen species, singlet oxygen sensor green.

References

Agati G, Guidi L, Landi M, Tattini M (2021) Anthocyanins in photoprotection: knowing the actors in play to solve this complex ecophysiological issue. New Phytologist 232, 2228-2235.
| Crossref | Google Scholar | PubMed |

Anderson R, Ryser P (2015) Early autumn senescence in red maple (Acer rubrum L.) is associated with high leaf anthocyanin content. Plants (Basel) 4, 505-522.
| Crossref | Google Scholar | PubMed |

Cheeseman JM (2009) Seasonal patterns of leaf H2O2 content: reflections of leaf phenology, or environmental stress? Functional Plant Biology 36, 721-731.
| Crossref | Google Scholar | PubMed |

Cooney LJ, Logan BA, Walsh MJL, Nnatubeugo NB, Reblin JS, Gould KS (2018) Photoprotection from anthocyanins and thermal energy dissipation in senescing red and green Sambucus canadensis peduncles. Environmental and Experimental Botany 148, 27-34.
| Crossref | Google Scholar |

Dani KGS, Pollastri S, Pinosio S, Reichelt M, Sharkey TD, Schnitzler J-P, Loreto F (2022) Isoprene enhances leaf cytokinin metabolism and induces early senescence. New Phytologist 234, 961-974.
| Crossref | Google Scholar | PubMed |

Davis GA, Kanazawa A, Schöttler MA, Kohzuma K, Froehlich JE, Rutherford AW, Satoh-Cruz M, Minhas D, Tietz S, Dhingra A, Kramer DM (2016) Limitations to photosynthesis by proton motive force-induced photosystem II photodamage. elife 5, e16921.
| Crossref | Google Scholar | PubMed |

Dodge JD (1970) Changes in chloroplast fine structure during the autumnal senescence of Betula leaves. Annals of Botany 34, 817-824.
| Crossref | Google Scholar |

García-Plazaola JI, Hernández A, Becerril JM (2003) Antioxidant and pigment composition during autumnal leaf senescence in woody deciduous species differing in their ecological traits. Plant Biology (Stuttg) 5, 557-566.
| Crossref | Google Scholar |

Greer DH, Berry JA, Björkman O (1986) Photoinhibition of photosynthesis in intact bean leaves: role of light and temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168, 253-260.
| Crossref | Google Scholar | PubMed |

Grennan AK, Ort DR (2007) Cool temperatures interfere with D1 synthesis in tomato by causing ribosomal pausing. Photosynthesis Research 94, 375-385.
| Crossref | Google Scholar | PubMed |

Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1706, 68-80.
| Crossref | Google Scholar | PubMed |

Hakala-Yatkin M, Sarvikas P, Paturi P, Mäntysaari M, Mattila H, Tyystjärvi T, Nedbal L, Tyystjärvi E (2011) Magnetic field protects plants against high light by slowing down production of singlet oxygen. Physiologia Plantarum 142, 26-34.
| Crossref | Google Scholar | PubMed |

Hughes NM, George CO, Gumpman CB, Neufeld HS (2022) Coevolution and photoprotection as complementary hypotheses for autumn leaf reddening: a nutrient-centered perspective. New Phytologist 233, 22-29.
| Crossref | Google Scholar | PubMed |

Junker LV, Ensminger I (2016) Relationship between leaf optical properties, chlorophyll fluorescence and pigment changes in senescing Acer saccharum leaves. Tree Physiology 36, 694-711.
| Crossref | Google Scholar | PubMed |

Keskitalo J, Bergquist G, Gardeström P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiology 139, 1635-1648.
| Crossref | Google Scholar |

Khorobrykh S, Havurinne V, Mattila H, Tyystjärvi E (2020) Oxygen and ROS in photosynthesis. Plants 9, 91.
| Crossref | Google Scholar | PubMed |

Kitao M, Yazaki K, Tobita H, Agathokleous E, Kishimoto J, Takabayashi A, Tanaka R (2022) Exposure to strong irradiance exacerbates photoinhibition and suppresses N resorption during leaf senescence in shade-grown seedlings of fullmoon maple (Acer japonicum). Frontiers in Plant Science 13, 1006413.
| Crossref | Google Scholar | PubMed |

Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209-218.
| Crossref | Google Scholar | PubMed |

Krieger-Liszkay A, Trösch M, Krupinska K (2015) Generation of reactive oxygen species in thylakoids from senescing flag leaves of the barley varieties Lomerit and Carina. Planta 241, 1497-1508.
| Crossref | Google Scholar | PubMed |

Krieger-Liszkay A, Krupinska K, Shimakawa G (2019) The impact of photosynthesis on initiation of leaf senescence. Physiologia Plantarum 166, 148-164.
| Google Scholar | PubMed |

Krupinska K, Mulisch M, Hollmann J, Tokarz K, Zschiesche W, Kage H, Humbeck K, Bilger W (2012) An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high-yield variety of barley. Physiologia Plantarum 144, 189-200.
| Crossref | Google Scholar | PubMed |

Kuai B, Chen J, Hörtensteiner S (2018) The biochemistry and molecular biology of chlorophyll breakdown. Journal of Experimental Botany 69, 751-767.
| Crossref | Google Scholar | PubMed |

Lehtimäki N, Shunmugam S, Jokela J, Wahlsten M, Carmel D, Keränen M, Sivonen K, Aro E-M, Allahverdiyeva Y, Mulo P (2011) Nodularin uptake and induction of oxidative stress in spinach (Spinachia oleracea). Journal of Plant Physiology 168, 594-600.
| Crossref | Google Scholar | PubMed |

Lepeduš H, Jurković V, Štolf I, Ćurković-Peric M, Fulgosi H, Cesar V (2010) Changes in photosystem II photochemistry in senescing maple leaves. Croatica Chemica Acta 83, 379-386.
| Google Scholar |

Lev-Yadun S (2022) The phenomenon of red and yellow autumn leaves: hypotheses, agreements and disagreements. Journal of Evolutionary Biology 35, 1245-1282 10.1111/jeb.14069.
| Google Scholar | PubMed |

Lihavainen J, Edlund E, Björkén L, Bag P, Robinson KM, Jansson S (2021) Stem girdling affects the onset of autumn senescence in aspen in interaction with metabolic signals. Physiologia Plantarum 172, 201-217.
| Crossref | Google Scholar | PubMed |

Mattila H, Tyystjärvi E (2023) Red pigments in autumn leaves of Norway maple do not offer significant photoprotection but coincide with stress symptoms. Tree Physiology 43, 751-768.
| Crossref | Google Scholar | PubMed |

Mattila H, Valev D, Havurinne V, Khorobrykh S, Virtanen O, Antinluoma M, Mishra KB, Tyystjärvi E (2018) Degradation of chlorophyll and synthesis of flavonols during autumn senescence – the story told by individual leaves. Annals of Botany PLANTS 10, ply028.
| Crossref | Google Scholar |

Mattila H, Mishra KB, Kuusisto I, Mishra A, Novotná K, Šebela D, Tyystjärvi E (2020) Effects of low temperature on photoinhibition and singlet oxygen production in four natural accessions of Arabidopsis. Planta 252, 19.
| Crossref | Google Scholar | PubMed |

Mattila H, Sotoudehnia P, Kuuslampi T, Stracke R, Mishra KB, Tyystjärvi E (2021) Singlet oxygen, flavonols and photoinhibition in green and senescing silver birch leaves. Trees – Structure and Function 35, 1267-1282.
| Crossref | Google Scholar |

Mattila H, Mishra S, Tyystjärvi T, Tyystjärvi E (2023) Singlet oxygen production by photosystem II is caused by misses of the oxygen evolving complex. New Phytologist 237, 113-125.
| Crossref | Google Scholar | PubMed |

Mesa T, Munné-Bosch S (2023) α-Tocopherol in chloroplasts: nothing more than an antioxidant? Current Opinion in Plant Biology 74, 102400.
| Crossref | Google Scholar | PubMed |

Moy A, Le S, Verhoeven A (2015) Different strategies for photoprotection during autumn senescence in maple and oak. Physiologia Plantarum 155, 205-216.
| Crossref | Google Scholar | PubMed |

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1767, 414-421.
| Crossref | Google Scholar | PubMed |

Niewiadomska E, Polzien L, Desel C, Rozpadek P, Miszalski Z, Krupinska K (2009) Spatial patterns of senescence and development-dependent distribution of reactive oxygen species in tobacco (Nicotiana tabacum) leaves. Journal of Plant Physiology 166, 1057-1068.
| Crossref | Google Scholar | PubMed |

Nikiforou C, Nikolopoulos D, Manetas Y (2011) The winter-red-leaf syndrome in Pistacia lentiscus: evidence that the anthocyanic phenotype suffers from nitrogen deficiency, low carboxylation efficiency and high risk of photoinhibition. Journal of Plant Physiology 168, 2184-2187.
| Crossref | Google Scholar | PubMed |

Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and nonphotochemical components—calculation of qP and Fv′/Fm′ without measuring Fo′. Photosynthesis Research 54, 135-142.
| Crossref | Google Scholar |

Pätsikkä E, Kairavuo M, Šeršen F, Aro E-M, Tyystjärvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiology 129, 1359-1367.
| Google Scholar | PubMed |

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta (BBA) – Bioenergetics 975, 384-394.
| Crossref | Google Scholar |

Quirino BF, Noh Y-S, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends in Plant Science 5, 278-282.
| Crossref | Google Scholar | PubMed |

Rantala M, Mulo P, Tyystjärvi E, Mattila H (2023) Biophysical and molecular characteristics of senescing leaves of two Norway maple varieties differing in anthocyanin content. Physiologia Plantarum 175, e13999.
| Crossref | Google Scholar | PubMed |

Raymond Hunt E, Jr, Daughtry CST (2014) Chlorophyll meter calibrations for chlorophyll content using measured and simulated leaf transmittances. Agronomy Journal 106, 931-939.
| Crossref | Google Scholar |

Renner SS, Zohner CM (2019) The occurrence of red and yellow autumn leaves explained by regional differences in insolation and temperature. New Phytologist 224, 1464-1471.
| Crossref | Google Scholar | PubMed |

Rise M, Cojocaru M, Gottlieb HE, Goldschmidt EE (1989) Accumulation of α-tocopherol in senescing organs as related to chlorophyll degradation. Plant Physiology 89, 1028-1030.
| Crossref | Google Scholar | PubMed |

Ruberti C, Barizza E, Bodner M, La Rocca N, De Michele R, Carimi F, Lo Schiavo F, Zottini M (2014) Mitochondria change dynamics and morphology during grapevine leaf senescence. PLoS ONE 9, e102012.
| Crossref | Google Scholar | PubMed |

Sasi JM, Gupta S, Singh A, Kujur A, Agarwal M, Katiyar-Agarwal S (2022) Know when and how to die: gaining insights into the molecular regulation of leaf senescence. Physiology and Molecular Biology of Plants 28, 1515-1534.
| Crossref | Google Scholar | PubMed |

Serôdio J, Campbell DA (2021) Photoinhibition in optically thick samples: effects of light attenuation on chlorophyll fluorescence-based parameters. Journal of Theoretical Biology 513, 110580.
| Crossref | Google Scholar | PubMed |

Shi D, Wei X, Chen G, Xu Y (2012) Changes in photosynthetic characteristics and antioxidative protection in male and female ginkgo during natural senescence. Journal of the American Society for Horticultural Science 137, 349-360.
| Crossref | Google Scholar |

Springer A, Acker G, Bartsch S, Bauerschmitt H, Reinbothe S, Reinbothe C (2015) Differences in gene expression between natural and artificially induced leaf senescence in barley. Journal of Plant Physiology 176, 180-191.
| Crossref | Google Scholar | PubMed |

Szymańska R, Kruk J (2008) Tocopherol content and isomers’ composition in selected plant species. Plant Physiology and Biochemistry 46, 29-33.
| Crossref | Google Scholar | PubMed |

Tyystjärvi E (2013) Photoinhibition of photosystem II. In ‘International review of cell and molecular biology. Vol. 300’. (Ed. KW Jeon) pp. 243–303. (Academic Press)

Uzarević Z, Štolfa I, Parađiković N, Cesar V, Lepeduš H (2011) Physiology and biochemistry of leaf bleaching in prematurely aging maple (Acer saccharinum L.) trees: I. Hydrogen peroxide level, antioxidative responses and photosynthetic pigments. Acta Botanica Croatica 70, 121-132.
| Crossref | Google Scholar |

Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1817, 209-217.
| Crossref | Google Scholar | PubMed |

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307-313.
| Crossref | Google Scholar |

Wingler A, Marès M, Pourtau N (2004) Spatial patterns and metabolic regulation of photosynthetic parameters during leaf senescence. New Phytologist 161, 781-789.
| Crossref | Google Scholar | PubMed |

Wingler A, Brownhill E, Pourtau N (2005) Mechanisms of the light-dependent induction of cell death in tobacco plants with delayed senescence. Journal of Experimental Botany 56, 2897-2905.
| Crossref | Google Scholar | PubMed |

Wojciechowska N, Marzec-Schmidt K, Kalemba EM, Zarzyńska-Nowak A, Jagodziński AM, Bagniewska-Zadworna A (2018) Autophagy counteracts instantaneous cell death during seasonal senescence of the fine roots and leaves in Populus trichocarpa. BMC Plant Biology 18, 260.
| Crossref | Google Scholar | PubMed |

Yu Z-C, Lin W, Zheng X-T, Chow WS, Luo Y-N, Cai M-L, Peng C-L (2021) The relationship between anthocyanin accumulation and photoprotection in young leaves of two dominant tree species in subtropical forests in different seasons. Photosynthesis Research 149, 41-55.
| Crossref | Google Scholar | PubMed |