Sunlight promotes aboveground carbon loss by producing polysaccharides from litter decomposition in a temperate forest

Lu Chang , Jiaojiao Deng , Juanjuan Zhang , Qinglong Fu , Tao Wang , Takashi Osono , Huan Peng , Thomas Matthew Robson , Hiroko Kurokawa , Qing-Wei Wang

Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 22

PDF
Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) :22 DOI: 10.1007/s11676-024-01811-w
Original Paper
research-article

Sunlight promotes aboveground carbon loss by producing polysaccharides from litter decomposition in a temperate forest

Author information +
History +
PDF

Abstract

Photodegradation is considered as a universal contributing factor to litter decomposition and carbon (C) cycling within the Earth’s biomes. Identifying how solar radiation modifies the molecular structure of litter is essential to understand the mechanism controlling its decomposition and reaction to shifts in climatic conditions and land-use. In this study, we performed a spectral-attenuation experiment following litter decomposition in an understory and gap of a temperate deciduous forest. We found that short-wavelength visible light, especially blue light, was the main factor driving variation in litter molecular structure of Fagus crenata Blume, Quercus crispula Blume, Acer carpinifolium Siebold & Zuccarini and Betula platyphylla Sukaczev, explaining respectively 56.5%, 19.4%, 66.3%, and 16.7% of variation in its chemical composition. However, the variation also depended on canopy openness: Only in the forest gap was lignin aromatic C negatively associated with C-oxygen (C–O) bonding in polysaccharides receiving treatments containing blue light of the full spectrum of solar radiation. Regardless of species, the decomposition index of litter that explained changes in mass and lignin loss was driven by the relative content of C–O stretching in polysaccharides and lignin aromatic C. The results suggest that the availability of readily degradable polysaccharides produced by the reduction in lignin aromatic C most plausibly explains the rate of litter photodegradation. Photo-products of photodegradation might augment the C pool destabilized by the input of readily degradable organic compounds (i.e., polysaccharides).

Keywords

Forest carbon cycling / Solar radiation / Photodegradation / Litter molecular structure / Fourier transform infrared (FTIR) spectroscopy

Cite this article

Download citation ▾
Lu Chang, Jiaojiao Deng, Juanjuan Zhang, Qinglong Fu, Tao Wang, Takashi Osono, Huan Peng, Thomas Matthew Robson, Hiroko Kurokawa, Qing-Wei Wang. Sunlight promotes aboveground carbon loss by producing polysaccharides from litter decomposition in a temperate forest. Journal of Forestry Research, 2025, 36(1): 22 DOI:10.1007/s11676-024-01811-w

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Adair EC, Parton WJ, Del Grosso SJ, Silver WL, Harmon ME, Hall SA, Burke IC, Hart SC. Simple three-pool model accurately describes patterns of long-term litter decomposition in diverse climates. Glob Change Biol, 2008, 14(11): 2636-2660

[2]

Almagro M, Martínez-López J, Maestre FT, Rey A. The contribution of photodegradation to litter decomposition in semiarid Mediterranean grasslands depends on its interaction with local humidity conditions, litter quality and position. Ecosystems, 2017, 20(3): 527-542

[3]

Aphalo PJ, Albert A, Björn LO, McLeod AR, Robson TM, Rosenqvist E (2012) Beyond the visible: A handbook of best practice in plant UV photobiology, First edn. COST Action FA0906 UV4growth, Finland, p 3

[4]

Austin AT, Ballaré CL. Dual role of lignin in plant litter decomposition in terrestrial ecosystems. Proc Natl Acad Sci USA, 2010, 107(10): 4618-4622

[5]

Austin AT, Ballaré CL. Photodegradation in terrestrial ecosystems. New Phytol, 2024, 244(3): 769-785

[6]

Austin AT, Vivanco L. Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation. Nature, 2006, 442(7102): 555-558

[7]

Austin AT, Méndez MS, Ballaré CL. Photodegradation alleviates the lignin bottleneck for carbon turnover in terrestrial ecosystems. Proc Natl Acad Sci USA, 2016, 113(16): 4392-4397

[8]

Barnes PW, Robson TM, Neale PJ, Williamson CE, Zepp RG, Madronich S, Wilson SR, Andrady AL, et al.. Environmental effects of stratospheric ozone depletion, UV radiation, and interactions with climate change: UNEP environmental effects assessment panel, update 2021. Photochem Photobiol Sci, 2022, 21(3): 275-301

[9]

Barnes PW, Robson TM, Zepp RG, Bornman JF, Jansen MAK, Ossola R, Wang QW, Robinson SA, et al.. Interactive effects of changes in UV radiation and climate on terrestrial ecosystems, biogeochemical cycles, and feedbacks to the climate system. Photochem Photobiol Sci, 2023, 22(5): 1049-1091

[10]

Berenstecher P, Vivanco L, Pérez LI, Ballaré CL, Austin AT. Sunlight doubles aboveground carbon loss in a seasonally dry woodland in Patagonia. Curr Biol, 2020, 30(16): 3243-3251.e3

[11]

Bradford MA, Berg B, Maynard DS, Wieder WR, Wood SA. Understanding the dominant controls on litter decomposition. J Ecol, 2016, 104(1): 229-238

[12]

Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, et al.. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett, 2008, 11(10): 1065-1071

[13]

Day TA, Bliss MS, Tomes AR, Ruhland CT, Guénon R. Desert leaf litter decay: coupling of microbial respiration, water-soluble fractions and photodegradation. Glob Chang Biol, 2018, 24(11): 5454-5470

[14]

Day TA, Urbine JM, Bliss MS. Supplemental precipitation accelerates decay but only in photodegraded litter and implications that sunlight promotes leaching loss. Biogeochemistry, 2022, 158(1): 113-129

[15]

Deng JJ, Fang S, Fang XM, Jin YQ, Kuang YW, Lin FM, Liu JQ, Ma JR, et al.. Forest understory vegetation study: current status and future trends. For Res, 2023

[16]

Erdenebileg E, Ye XH, Wang CW, Huang ZY, Liu GF, Cornelissen JHC. Positive and negative effects of UV irradiance explain interaction of litter position and UV exposure on litter decomposition and nutrient dynamics in a semi-arid dune ecosystem. Soil Biol Biochem, 2018, 124: 245-254

[17]

Faix O. Classification of lignins from different botanical origins by FT-IR spectroscopy. Holzforschung, 1991, 45(s1): 21-28

[18]

Farnet Da Silva AM, Foli L, Boudenne JL, Ziarelli F, Rebufa C. Photodegradation of typical Mediterranean plant litters: variations with Quercus species and the leaf-surface exposed. Eur J for Res, 2023, 142(2): 275-286

[19]

Frouz J, Cajthaml T, Mudrák O. The effect of lignin photodegradation on decomposability of Calamagrostis epigeios grass litter. Biodegradation, 2011, 22(6): 1247-1254

[20]

Fukushima RS, Hatfield RD. Extraction and isolation of lignin for utilization as a standard to determine lignin concentration using the acetyl bromide spectrophotometric method. J Agric Food Chem, 2001, 49(7): 3133-3139

[21]

Gliksman D, Haenel S, Osem Y, Yakir D, Zangy E, Preisler Y, Grünzweig JM. Litter decomposition in Mediterranean pine forests is enhanced by reduced canopy cover. Plant Soil, 2018, 422(1): 317-329

[22]

Hartikainen SM, Pieristè M, Lassila J, Robson TM. Seasonal patterns in spectral irradiance and leaf UV-a absorbance under forest canopies. Front Plant Sci, 2020, 10: 1762

[23]

Hu J, Kang LY, Li ZL, Feng XH, Liang CF, Wu Z, Zhou W, Liu XN, Yang YH, Chen LY. Photo-produced aromatic compounds stimulate microbial degradation of dissolved organic carbon in thermokarst lakes. Nat Commun, 2023, 14(1): 3681

[24]

Jiang H, Pan YT, Liang JW, Yang YH, Chen Q, Lv MQ, Pang L, He WH, Tian XJ. UV radiation doubles microbial degradation of standing litter in a subtropical forest. J Ecol, 2022, 110(92156-2166

[25]

Jiang H, Yang YH, Liang JW, Lv MQ, Tian XJ. Standing decomposition of dead leaves in winter and its legacy effects should not be ignored in subtropical forests. Plant Soil, 2023, 492(1485-499

[26]

Jolliffe IT (2009) Principal component analysis for special types of data. In: Principal component analysis. springer Series in Statistics. Springer-Verlag, New York pp 338–372

[27]

Keiser AD, Warren R, Filley T, Bradford MA. Signatures of an abiotic decomposition pathway in temperate forest leaf litter. Biogeochemistry, 2021, 153(2): 177-190

[28]

Lammers K, Arbuckle-Keil G, Dighton J. FT-IR study of the changes in carbohydrate chemistry of three New Jersey pine barrens leaf litters during simulated control burning. Soil Biol Biochem, 2009, 41(2): 340-347

[29]

Lehmann J, Kleber M. The contentious nature of soil organic matter. Nature, 2015, 528(7580): 60-68

[30]

Lei WY, Pan Q, Teng PJ, Yu JC, Li N. How does soil organic matter stabilize with soil and environmental variables along a black soil belt in Northeast China? An explanation using FTIR spectroscopy data. Catena, 2023, 228: 107152

[31]

Li K, Lu Y, Wang QW, Ni R, Han R, Li CR, Zhang CH, Shen WX, et al.. Leaf litter mixtures alter decomposition rate, nutrient retention, and bacterial community composition in a temperate forest. For Res, 2023

[32]

Li WS, Liu ZY, Zhao JF, Ma LF, Wu JH, Qi JF, Wang H. Leaf mechanical properties as potential predictors of leaf-litter decomposability. For Re, 2023

[33]

Li XZ, Wang YN, Zhang JJ, Robson TM, Kurokawa H, Peng H, Zhou L, Yu DP, Deng JJ, Wang QW. Autumn sunlight promotes aboveground carbon loss in a temperate mixed forest. Ecol Process, 2024, 13(1): 48

[34]

Lin Y, King JY, Karlen SD, Ralph J. Using 2D NMR spectroscopy to assess effects of UV radiation on cell wall chemistry during litter decomposition. Biogeochemistry, 2015, 125(3427-436

[35]

Madari BE, Reeves JB, Machado PLOA, Guimarães CM, Torres E, McCarty GW. Mid- and near-infrared spectroscopic assessment of soil compositional parameters and structural indices in two Ferralsols. Geoderma, 2006, 136(1–2245-259

[36]

Marinho OA, Martinelli LA, Duarte-Neto PJ, Mazzi EA, King JY. Photodegradation influences litter decomposition rate in a humid tropical ecosystem. Brazil Sci Total Environ, 2020, 715: 136601

[37]

Méndez MS, Ballaré CL, Austin AT. Dose-responses for solar radiation exposure reveal high sensitivity of microbial decomposition to changes in plant litter quality that occur during photodegradation. New Phytol, 2022, 235(5): 2022-2033

[38]

Ni XY, Berg B, Yang WQ, Li H, Liao S, Tan B, Yue K, Xu ZF, Zhang L, Wu FZ. Formation of forest gaps accelerates C, N and P release from foliar litter during 4 years of decomposition in an alpine forest. Biogeochemistry, 2018, 139(3321-335

[39]

Pieristè M, Chauvat M, Kotilainen TK, Jones AG, Aubert M, Robson TM, Forey E. Solar UV-a radiation and blue light enhance tree leaf litter decomposition in a temperate forest. Oecologia, 2019, 191(1): 191-203

[40]

Ranade SS, García-Gil MR. Lignin biosynthesis pathway repressors in gymnosperms: differential repressor domains as compared to angiosperms. For Res, 2024

[41]

Saparrat MCN, Estevez JM, Troncozo MI, Arambarri AM, Balatti PA. In-vitro depolymerization of Scutia buxifolia leaf-litter by a dominant Ascomycota Ciliochorella sp.. Int Biodeterior Biodegrad, 2010, 64(3): 262-266

[42]

Song XZ, Zhang HL, Jiang H, Peng CH. Combination of nitrogen deposition and ultraviolet-B radiation decreased litter decomposition in subtropical China. Plant Soil, 2014, 380(1): 349-359

[43]

Soong JL, Calderón FJ, Betzen J, Cotrufo MF. Quantification and FTIR characterization of dissolved organic carbon and total dissolved nitrogen leached from litter: a comparison of methods across litter types. Plant Soil, 2014, 385(1): 125-137

[44]

Tang GR, Zhang H, Xing HL, Yuan TH, Gontcharov AA, Yang L. Light adaptation strategies of Quercus mongolica at different ages in four plantations. For Res, 2024

[45]

Wan P, He RR. Canopy structure and understory light characteristics of a natural Quercus aliena var. acuteserrata forest in China northwest: influence of different forest management methods. Ecol Eng, 2020, 153: 105901

[46]

Wan P, Zhang GQ, Wang HX, Zhao ZH, Hu YB, Zhang GG, Hui GY, Liu WZ. Impacts of different forest management methods on the stand spatial structure of a natural Quercus aliena var. acuteserrata forest in Xiaolongshan. China Ecol Inform, 2019, 50: 86-94

[47]

Wang XQ, Ren HQ. Surface deterioration of moso bamboo (Phyllostachys pubescens) induced by exposure to artificial sunlight. J Wood Sci, 2009, 55(1): 47-52

[48]

Wang QW, Pieristè M, Liu CG, Kenta T, Robson TM, Kurokawa H. The contribution of photodegradation to litter decomposition in a temperate forest gap and understorey. New Phytol, 2021, 229(5): 2625-2636

[49]

Wang QW, Robson TM, Pieristè M, Kenta T, Zhou WM, Kurokawa H. Canopy structure and phenology modulate the impacts of solar radiation on C and N dynamics during litter decomposition in a temperate forest. Sci Total Environ, 2022, 820: 153185

[50]

Wang QW, Pieristè M, Kotilainen TK, Forey E, Chauvat M, Kurokawa H, Robson TM, Jones AG. The crucial role of blue light as a driver of litter photodegradation in terrestrial ecosystems. Plant Soil, 2023, 488(1): 23-38

[51]

Xie LL, Yang YM, Ma JR, Lin GG, Deng JJ, Robson TM, Peng H, Zhou L, Yu DP, Wang QW. Variations in ectomycorrhizal exploration types parallel seedling fine root traits of two temperate tree species under extreme drought and contrasting solar radiation treatments. Plant Cell Environ, 2024, 47(125053-5066

[52]

Yamada T, Yoshioka A, Hashim M, Liang NS, Okuda T. Spatial and temporal variations in the light environment in a primary and selectively logged forest long after logging in Peninsular Malaysia. Trees, 2014, 28(5): 1355-1365

[53]

Yao B, Zeng XY, Pang L, Kong XS, Tian K, Ji YL, Sun SC, Tian XJ. The photodegradation of lignin methoxyl C promotes fungal decomposition of lignin aromatic C measured with 13C-CPMAS NMR. J Fungi, 2022, 8(9900

[54]

Zhang JJ, Kang L, Cao Y, Zhang CH, Wang QW. Litter decomposition in pure and mixed plantations on the Loess Plateau, China: lack of home-field advantage. CATENA, 2024, 244: 108239

[55]

Zhao YJ, Abid M, Xie XX, Fu YL, Huang YX, Cai ZY, Lin HN. Harnessing unconventional monomers to tailor lignin structures for lignocellulosic biomass valorization. For Res, 2024

RIGHTS & PERMISSIONS

The Author(s)

PDF

481

Accesses

0

Citation

Detail

Sections
Recommended

/