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Non-Structural Carbohydrates Regulated by Season and Species In www.nature.com/scientificreports OPEN Non-structural carbohydrates regulated by season and species in the subtropical monsoon broad- Received: 6 September 2017 Accepted: 27 December 2017 leaved evergreen forest of Yunnan Published: xx xx xxxx Province, China Wande Liu1,2, Jianrong Su1,2, Shuaifeng Li1,2, Xuedong Lang1,2 & Xiaobo Huang1,2 Non-structural carbohydrates (NSC) play important roles in adapting to environments in plants. Despite extensive research on the seasonal dynamics and species diferences of NSC, the relative contributions of season and species to NSC is not well understood. We measured the concentration of starch, soluble sugar, NSC, and the soluble sugar:starch ratio in leaves, twigs, trunks and roots of twenty dominant species for dry and wet season in monsoon broad-leaved evergreen forest, respectively. The majority of concentration of NSC and starch in the roots, and the leaves contained the highest concentration of soluble sugar. A seasonal variation in starch and NSC concentrations higher in the dry season. Conversely, the wet season samples had higher concentration of soluble sugar and the sugar:starch ratio. Signifcant diferences exist for starch, soluble sugar and NSC concentrations and the sugar:starch ratio across species. Most species had higher starch and NSC concentrations in the dry season and higher soluble sugar concentration and the sugar:starch ratio in wet season. Repeated variance analysis showed that starch and NSC concentrations were strongly afected by season although the efect of seasons, species, and the interaction of the two on the starch, soluble sugar, and NSC concentrations were signifcant. Non-structural carbohydrates (NSC) are the primary photosynthates and the key regulators of the physiological adjustment of plants to environmental stress1–4. In addition, NSC provide substrates for growth and metabolism5,6 and therefore play vital roles in plant’s life processes7. Te NSC level of a plant is an important indicator of the carbon source and sink capacity of vegetation8–10, and can further inform on plant growth3, bufering capacity, and adaptation strategies11. Hence, quantitative studies of the contribution of NSC to the carbon balance are of crucial importance to understand the survival and growth of plants. Te amounts of non-structural carbohydrates exhibit seasonal trends in order to adapt to seasonal resource variation, such as water, light, temperature, and nutrient availability. Seasonal dynamics of NSC have been stud- ied extensively in most of forest ecosystems. Hoch12 reports the highest concentrations in starch, soluble sugar, and NSC in leaves in early summer for deciduous species. In contrast, evergreen conifer trees had hardly any change for soluble sugar in leaves throughout the season. Similarly, the NSC in stem sapwood varied very little throughout the season12. While yellow birch and sugar maple seedlings had the highest total NSC and starch by the end of the growing season13. In Mediterranean regions, NSC concentration of deciduous Aesculus califor- nica dropped during fruit production in fall and re-growth in early spring, whereas evergreen Quercus agrifolia showed little change throughout the year14. For the tropical forests, Würth et al.2 reports NSC showed a dry sea- son (dormant period) maximum and a wet season (growing season) minimum in 17 tropical trees. Newell et al.15 also reports the highest NSC concentrations in dormant period for tropical pioneer species, whereas later succes- sion evergreen species showed smaller or non-signifcant seasonal changes in NSC concentration. In subtropical regions, Bullock16 found the NSC of Jacaratia mexicana in stem increased in the end of the rainy season, whereas 1Research Institute of Resources Insects, Chinese Academy of Forestry, Kunming, 650224, China. 2Pu’er Forest Eco- system Research Station, China’s State Forestry Administration, Kunming, 650224, China. Correspondence and requests for materials should be addressed to J.S. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:1083 | DOI:10.1038/s41598-018-19271-8 1 www.nature.com/scientificreports/ Figure 1. Te concentration of starch, soluble sugar, and non-structural carbohydrates for the leaves, twigs, trunks and roots across all seasons. Spondias purpurea showed little change throughout the year. Although seasonal variation in NSCs concentrations is well-documented in most of forest ecosystems, the seasonal trend of NSCs continues to be a subject of active research and some controversy and the relative contributions of seasonal efects to the dynamics of NSC are not well understood. Te dynamics and concentration of NSC display diferences across species within the same region that is related to their diferent life forms or ecological strategies15,17–20. Te concentrations of NSC and their components difered signifcantly among species and tissues for three temperate tree species in Northeast China21. Similar results were found among other temperate species12,13,22,23, Mediterranean species20, and tropical species2, but the dynamics of NSC also display species specifc diference. Several authors have reported diferences in the carbohydrate dynamics of deciduous and evergreen species15, and most ofen evergreen species display less dra- matic seasonal fuctuations of their carbohydrate reserves than deciduous species12. In deciduous plants, NSC is mobilized from the perennial structures to support tissue growth and respiration in early spring, resulting in decreased concentrations of NSC in these storage organs24. In woody plants, sugars accumulate from autumn to winter25. It has been observed that maximum sugar concentrations are found in poplars in the winter26,27. In some herbaceous plants, researchers have also found that changes in sugar concentrations are correlated with sea- son22. Terefore, Te concentration and dynamics of NSC may be infuenced by the species and their taxonomic relationships28. Although NSC seasonal dynamics and species diferences in tropical, temperate and Mediterranean forests ecosystems have been studied, the efect of season and species on NSC have not been well characterized in sub- tropical forests ecosystems. Most evergreen species should display less dramatic seasonal fuctuations in NSC because seasonal variation in carbon gain may be less common for evergreen species in subtropical forests than in temperate forests. In this study, we hypothesize that the NSC in the subtropical monsoon broad-leaved evergreen forest exhibits the greatest seasonal changes due to seasonal precipitation reduction. Precipitation chiefy occurs in the wet season between May and October, and not as frequently during the dry season (from November to April) in Pu’er region of Yunnan Province, China29. We also hypothesize that: (1) greatest species fuctuations in NSC concentrations will occur, and (2) the efect of season on the NSC will be higher than species because all species are afected by the season. Tese hypotheses were tested by seasonally measuring NSC and its component concentrations in leaves, twigs, trunks and roots of twenty of the most abundant species growing in the sub- tropical monsoon broad-leaved evergreen forest of Yunnan Province, China. Te repeated measures analysis of variance was used to distinguish the efect of season and species on NSC, which allows for a more detailed picture of the efect of season and species on NSC. Results NSC allocation among tissues. Starch, soluble sugar and NSC concentrations varied signifcantly among four tissues across all seasons (Fig. 1). Te highest starch and NSC concentrations were found in the roots, while the leaves had the lowest starch concentrations. No signifcant diferences were found for starch concentrations between twigs and trunks and for NSC concentrations among leaves, twigs and trunks (p > 0.05). Te largest sol- uble sugar concentration was found to be in the leaves, closely followed by twigs and then roots, and lastly trunks; there were no signifcant diferences between twigs and roots (p > 0.05). Seasonal diferences for NSC. Dramatic variation in the concentration of starch, soluble sugar and NSC and the ratio of soluble sugar to starch occurred between dry and wet seasons (Table 1). Te dry season had the higher concentrations of starch and NSC than the wet season. However, the concentration of soluble sugar and the ratio of soluble sugar to starch were higher in the wet season than dry season (Table 1). Signifcant seasonal diferences were found for the concentration of starch, soluble sugar and NSC and the ratio of soluble sugar to starch in four tissues (leaf, twig, trunk and root) (Fig. 2). Te concentration of starch and NSC were higher in the dry season than in wet season for all four tissues. But the concentration of soluble sugar SCIENTIFIC REPORTS | (2018) 8:1083 | DOI:10.1038/s41598-018-19271-8 2 www.nature.com/scientificreports/ Indicators Seasons Mean ± SE(%) Dry season 13.76 ± 0.33a Starch Wet season 3.52 ± 0.07b Dry season 3.28 ± 0.07a Soluble sugar Wet season 4.16 ± 0.05b Dry season 17.05 ± 0.33a NSC Wet season 7.69 ± 0.09b Te ratio of soluble Dry season 0.42 ± 0.03a sugar to starch Wet season 1.51 ± 0.03b Table 1. Changes of starch, soluble sugar, non-structural carbohydrates, and the ratio of soluble sugar to starch in diferent seasons. Diferent letters in the same row indicate signifcant diferences afer Bonferroni’s post-hoc test (p < 0.05). Figure 2. Te concentration of starch, soluble sugar, and non-structural carbohydrates and the ratio of soluble sugar to starch for the leaves, twigs, trunks and roots in dry season and wet season, open bars represent the dry season, and the closed bars are the wet season, ** and *** indicate signifcant diference at the 0.01 level and the 0.001 level, respectively. and the ratio of soluble sugar to starch were higher in the wet season than in dry season for all four tissues except for the concentration of soluble sugar in leaf (Fig. 2). Species diferences for NSC. Signifcant diferences existed among species for the concentration of starch (F = 3.709, p < 0.000), soluble sugar (F = 7.398, p < 0.000) and NSC (F = 5.125, p < 0.000) and the ratio of soluble sugar to starch (F = 4.653, p < 0.000, Table 2).
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