Chin J Plan Ecolo ›› 2016, Vol. 40 ›› Issue (6): 585-593.doi: 10.17521/cjpe.2015.0292

• Research Articles • Previous Articles     Next Articles

Effects of long-term flooding on respiratory metabolism of Taxodium ‘Zhongshansha 118’ seedlings

Yan-Ting ZHANG1, Jian-Jun ZHANG1,*(), Jian-Xiu WANG2, Xiao-Hong WU3, Bao-Qiang CHEN1, Peng-Fei LI1, Zhi-Zhen WANG1   

  1. 1School of Soil and Water Conservation, Beijing Forestry University, Beijing 100083, China

    2Forest Bureau in Kai County, Kai County, Chongqing 405400, China

    3Chongqing Hejia Spice Plant Limited Company, Chongqing 404000, China
  • Received:2015-08-11 Accepted:2016-03-26 Online:2016-06-15 Published:2016-06-30
  • Contact: Jian-Jun ZHANG


Aims Taxodium ‘Zhongshansha’ had a strong submergence tolerance, but the biological mechanism is not clearly defined. The respiratory metabolism for the tolerance of Taxodium ‘Zhongshansha 118’ ((Taxodium distichum × Taxodium mucronatum) × Taxodium mucronatum) to long-term flooding was investigated through the measuring and analyzing the changes in root starch and soluble sugar as well as the contents of anaerobic respiration enzymes, including lactic dehydrogenase (LDH), ethanol dehydrogenase (ADH) and pyruvate decarboxylase (PDC)), in the ‘Zhongshansha 118’ seedling. The biomass and activities of the seedling roots were also measured and analyzed.Methods 24 1-year Taxodium ‘Zhongshansha 118’ seedlings were randomly and equally divided into four groups and each group experienced one of four different levels of flooding (i.e., no flooding, waterlogging, partial submergence, deep submergence) from August 8 to November 8, 2014.Important findings The results showed that the contents of the anaerobic respiration enzymes in the seedling roots and leaves are increasing with the levels of severity of flooding, which indicated the roots and leaves adapt to long-term flooding by reinforcing their anaerobic respiration and activities of ADH that were higher than LDH for roots and leaves used in alcoholic fermentation mainly. The activities of anaerobic respiration enzymes in leaves were higher than that in roots, while leaves were more sensitive to flooding. The starch and soluble sugar in roots and leaves had similar trend with anaerobic respiration enzymes. However, roots starch was higher than leaves where soluble sugar was lower than roots. The higher content of starch were the important reason of strong submergence tolerance, and we consider the strategy to fit into long-term flooding is patience type. The paper demonstrate Taxodium ‘Zhongshansha 118’ have the physiological and the morphological properties to adapt to long-term flooding, including aerial root and basal part of stem expanded and the outer wall of the root lignified to protect the roots from flooding.

Key words: flooding stress, anaerobic respiration enzymes, soluble sugar, flooding tolerance, Taxodium ‘Zhongshansha’

Table 1

The underground part biomass of Taxodium ‘Zhongshansha 118’ after 93 d flooding (mean ± SD)"

Root mass (g)
Root length (cm)
Root surface area (cm2)
Root fractal dimension
对照 Control 10.23 ± 3.03a 873 ± 101a 256 ± 87a 1.67 ± 0.05a
水浸 Waterlogging 7.59 ± 1.21a 666 ± 105b 227 ± 94a 1.60 ± 0.09a
浅淹 Partial submergence 7.89 ± 0.94a 655 ± 114b 236 ± 59a 1.63 ± 0.04a
深淹 Deep submergence 5.26 ± 0.54a 508 ± 99c 164 ± 87a 1.61 ± 0.07a

Fig. 1

The changes of aerial root and basal part of stem in Taxodium ‘Zhongshansha 118’ under flooding treatments."

Table 2

Overground part biomass of Taxodium ‘Zhongshansha 118’ after 93 d flooding (mean ± SD)"

株高 Stem height (cm) 地径 Ground diameter (cm) 地上部分鲜质量
Fresh mass of overground part (g)
Root mass/fresh mass of overground part
After flooding
对照 Control 47 ± 3.6a 48 ± 4.2a 0.65 ± 0.02a 0.61 ± 0.06a 35.78 ± 9.71a 0.29a
水浸 Waterlogging 39 ± 4.1a 34 ± 5.5b 0.58 ± 0.02a 0.55 ± 0.02b 29.56 ± 6.45b 0.26a
浅淹 Partial submergence 47 ± 3.9a 38 ± 2.1b 0.62 ± 0.03a 0.57 ± 0.04b 18.21 ± 2.49c 0.43b
深淹 Deep submergence 38 ± 6.8a 31 ± 3.3b 0.62 ± 0.04a 0.53 ± 0.09b 12.99 ± 3.66d 0.33c

Fig. 2

Effect on root activity of Taxodium ‘Zhongshansha 118’ during long-term flooding (mean ± SD). Different lowercase letters indicate significant difference (p < 0.05)."

Fig. 3

Effect on anaerobic respiration enzymes of Taxodium ‘Zhongshansha 118’ during long-term flooding (mean ± SD). Capital letters indicate significant difference among groups (p < 0.05) and lowercase letters indicate significant difference in intra-group (p < 0.05)."

Fig. 4

Effect on soluble sugar and starch of Taxodium ‘Zhongshansha 118’ during long-term flooding (mean ± SD). Capital letters indicate significant difference among groups (p < 0.05) and lowercase letters indicate significant difference in intra-group (p < 0.05)."

Table 3

Effect on soluble sugar and starch conversion of Taxodium ‘Zhongshansha 118’ during long-term flooding (mean ± SD)"

淀粉+可溶性糖 Starch + soluble sugar 根/(根+叶) Root/(root + leaf) (%)
根系 Root 叶片 Leaf 淀粉 Starch 可溶性糖 Soluble sugar
对照 Control 65.38 ± 3.01a 41.07 ± 2.83a 62.42 ± 2.40a 39.88 ± 3.80a
水浸 Waterlogging 78.85 ± 4.57b 47.41 ± 3.10b 62.78 ± 2.30a 47.56 ± 3.10b
浅淹 Partial submergence 87.83 ± 2.34c 55.86 ± 3.75c 61.82 ± 2.40a 47.29 ± 2.30b
深淹 Deep submergence 95.71 ± 4.58d 68.71 ± 4.21d 58.76 ± 0.10a 46.73 ± 3.20b
[1] Akman M, Bhikharie AV, McLean EH, Boonman A, Visser EJ, Schranz ME (2012). Wait or escape? Contrasting submergence tolerance strategies of Rorippa amphibia, Rorippa sylvestris and their hybrid.Annals of botany, 109, 1263-1276.
[2] Angelov MN, Sung S-JS, Doong RL, Harms WR, Kormanik PP, Clanton C, Black J (1996). Long- and short-term flooding effects on survival and sink—Source relationships of swamp-adapted tree species.Tree Physiology, 16, 477-484.
[3] Botondi R, Russo V, Mencarelli F (2012). Anaerobic metabolism during short and long term storage of kiwifruit.Postharvest Biology and Technology, 64, 83-90.
[4] Candan N, Tarhan L (2012). Tolerance or sensitivity responses of Mentha pulegium to osmotic and waterlogging stress in terms of antioxidant defense systems and membrane lipid peroxidation.Environmental and Experimental Botany, 75, 83-88.
[5] Castonguay Y, Nadeau P, Simard RR (1993). Effects of flooding on carbohydrate and ABA levels in roots and shoots of alfalfa.Plant, Cell & Environment, 16, 695-702.
[6] Crawford RM (2003). Seasonal differences in plant responses to flooding and anoxia.Canadian Journal of Botany, 81, 1224-1246.
[7] Cuiying L, Tuanhui B, Fengwang M, Mingyu H (2010). Hypoxia tolerance and adaptation of anaerobic respiration to hypoxia stress in two Malus species.Scientia Horticulturae, 124, 274-279.
[8] de Oliveira VC, Joly CA (2009). Flooding tolerance of Calophyllum brasiliense Camb. (Clusiaceae): Morphological, physiological and growth responses.Trees, 24, 185-193.
[9] Fan DY, Xiong GM, Zhang AY, Liu X, Xie ZQ, Li ZJ (2015). Effect of water-lever regulation on species selection for ecological restoration practice in the water-level fluctuation zone of Three Gorges Reservoir.Chinese Journal of Plant Ecology, 39, 416-432. (in Chinese with English abstract)[樊大勇, 熊高明, 张爱英, 刘曦, 谢宗强, 李兆佳 (2015). 三峡库区水位调度对消落带生态修复中物种筛选实践的影响. 植物生态学报, 39, 416-432.]
[10] Ferner E, Rennenberg H, Kreuzwieser J (2012). Effect of flooding on C metabolism of flood-tolerant (Quercus robur) and non-tolerant (Fagus sylvatica) tree species.Tree Physiology, 32, 135-145.
[11] Gravatt DA, Kirby CJ (1998). Patterns of photosynthesis and starch allocation in seedlings of four bottomland hardwood tree species subjected to flooding.Tree Physiology, 18, 411-417.
[12] Hua JF, Hu LJ, Du LJ, Xu JH, Yin YL (2011a). Effects of soil water conditions on photosynthetic characteristics of Taxodium ‘Zhongshanshan 406’.Ecology and Environmental Sciences, 20(8-9), 1221-1225. (in Chinese with English abstract)[华建峰, 胡李娟, 杜丽娟, 徐建华, 殷云龙 (2011). 水分条件对中山杉406光合特性的影响. 生态环境学报, 20(8-9), 1221-1225.]
[13] Hua JF, Yin YL, Zhou DQ, Yu CG, Xu JH (2011b). Effects of soil water conditions on growth and physiology of Taxodium ‘Zhongshanshan 406’.Journal of Ecology and Rural Environment, 27, 50-54. (in Chinese with English abstract)[华建峰, 殷云龙, 周冬琴, 於朝广, 徐建华 (2011). 不同水分条件对中山杉406生长与生理的影响. 生态与农村环境学报, 27, 50-54.]
[14] Jackson MB, Ram PC (2003). Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence.Annals of botany, 91, 227-241.
[15] Johnson JR, Cobb BC, Drew MC (1994). Hypoxic induction of anoxia tolerance in roots of Adh1 null Zea mays L.Plant Physiology, 105, 61-67.
[16] King AR, Arnold MA (2012). Developmental stage and growth regulator concentration differentially affect vegetative propagation of select clones of Taxodium Rich.Hortscience, 47, 238-248.
[17] Liu Y (2013). Cultivation and management of Ascendens mucronatum in middle and lower Yangtze River.Modern Horticulture, (10), 22-24. (in Chinese with English abstract)[刘艳 (2013). 论长江中下游中山杉的栽培与管理. 现代园艺, (10), 22-24.]
[18] Liu Y, Willison JH (2013). Prospects for cultivating white mulberry (Morus alba) in the drawdown zone of the Three Gorges Reservoir, China.Environmental Science and Pollution Research International, 20, 7142-7151.
[19] Liu Z, Cheng R, Xiao W, Guo Q, Wang Y, Wang N, Wang Y (2015). Leaf gas exchange, chlorophyll fluorescence, non-structural carbohydrate content and growth responses of Distylium chinense during complete submergence and subaerial re-emergence.Aquatic Botany, 124, 70-77.
[20] Molina-Montenegro MA, Gallardo-Cerda J, Flores TSM, Atala C (2012). The trade-off between cold resistance and growth determines the Nothofagus pumilio treeline.Plant Ecology, 213, 133-142.
[21] Oren R, Sperry JS, Ewers BE, Pataki DE, Phillips N, Megonigal JP (2001). Sensitivity of mean canopy stomatal conductance to vapor pressure deficit in a flooded Taxodium distichum L. forest: Hydraulic and non-hydraulic effects.Oecologia, 126, 21-29.
[22] Parvin D, Karmoker JL (2013). Effects of waterlogging on ion accumulation and sugar, protein and proline contents in Corchorus capsularis.Bangladesh Journal of Botany, 42, 55-63.
[23] Rivoal J, Hanson AD (1994). Metabolic control of anaerobic glycolysis—Overexpression of lactate dehydrogenase in transgenic tomato root supports the Davies-Roberts hypothesis and points to a critical role for lactate secretion.Plant Physiology, 106, 1179-1185.
[24] Sairam, Kumutha D, Ezhilmathi K, Deshmukh PS, Srivastava GC (2008). Physiology and biochemistry of waterlogging tolerance in plants.Biologla Plantarum, 52, 401-412.
[25] Sauter M (2013). Root responses to flooding.Current Opinion in Plant Biology, 16, 282-286.
[26] Shi MF, Zeng B, Shen JH, Lei ST, Zhu Z, Liu JH (2010). A review of the correlation of flooding adaptability and carbohydrates in plants. Chinese Journal of Plant Ecology, 34, 855-866. (in Chinese with English abstract)[施美芬, 曾波, 申建红, 类淑桐, 朱智, 刘建辉 (2010). 植物水淹适应与碳水化合物的相关性. 植物生态学报, 34, 855-866.]
[27] Tang LZ, Huang BL, Haibara K, Toda H (2008) Ecologicaladaptation mechanisms of roots to flooded soil and respiration characteristics of knee roots of Taxodium ascendens. Journal of Plant Ecology (Chinese Version), 32, 1258-1267. (in Chinese with English abstract)[唐罗忠, 黄宝龙, 生原喜久雄, 户田浩人 (2008). 高水位条件下池杉根系的生态适应机制和膝根的呼吸特性. 植物生态学报, 32, 1258-1267.]
[28] Visser E, Bogemann GM, Steeg H, Pierik R, Blom C (2000). Flooding tolerance of Carex species in relation to field distribution and aerenchyma formation.New Phytologist, 148, 93-103.
[29] Voesenek LA, Bailey-Serres J (2013). Flooding tolerance: O2 sensing and survival strategies.Current Opinion in Plant Biology, 16, 647-653.
[30] Wang B, Jiang Y, Wang MC, Dong MY, Zhang YP (2015). Variations of non-structural carbohydrate concentration of Picea meyeri at different elevations of Luya Mountain, China.Chinese Journal of Plant Ecology, 39, 746-752. (in Chinese with English abstract)[王彪, 江源, 王明昌, 董满宇, 章异平 (2015). 芦芽山不同海拔白杄非结构性碳水化合物含量动态. 植物生态学报, 39, 746-752.]
[31] Yemm BEW, Willis AJ (1954). The estimation of carbohydrates in plant extracts by anthrone.Biochemical Journal, 57, 508-514.
[32] Yin YL, Yu CG, Hua JF, Huan JJ, Han LW, Qi BY, Ren P, Wu XH, Qi XC (2014). A trial on the silviculture of Taxodium hybrid ‘Zhonshanshan118’ planted in the hydro-fluctuation belt of the Three Gorges Reservoir within the Wanzhou district area of Chongqing City.China Forestry Science and Technology, 28(2), 110-114. (in Chinese with English abstract)[殷云龙, 於朝广, 华建峰, 环姣姣, 韩路弯, 亓白岩, 任凭, 吴晓洪, 祁小川 (2014). 重庆万州三峡库区消落带中山杉造林实验. 林业科技开发, 28(2), 110-114.]
[33] Zhang YT, Zhang JJ, Wu XH, Wang JX, Duan FP (2015). Flooding tolerance of Taxodium hybrid ‘Zhongshanshan’ along the hydro-fluctuation belt of the Three Gorges Reservoir.Science of Soil and Water Conservation,13(2), 56-62. (in Chinese with English abstract)[张艳婷, 张建军, 吴晓洪, 王建修, 段丰沛 (2015). 长江三峡库区消落带中山杉耐淹试验. 中国水土保持科学, 13(2), 56-62.]
[34] Zhou J, Tian X, Qiao L, Qin P (2012). Respiratory enzyme activity and regulation of respiration pathway in seashore mallow (Kosteletzkya virginica) seedlings under waterlogging conditions.Australian Journal of Crop Science, 6, 756-762.
[1] Yang Xiaoqing,Huang Xiaoqin,Han Xiaoyang,Liu Tengfei,Yue Xiaowei,Yi Ran. Effect of Exogenous Substances on Cold Tolerance and Key Sucrose Metabolic Gene Expression in Camellia sinensis [J]. Chin Bull Bot, 2020, 55(1): 21-30.
[2] WANG Biao,JIANG Yuan,WANG Ming-Chang,DONG Man-Yu,ZHANG Yi-Ping. Variations of non-structural carbohydrate concentration of Picea meyeri at different elevations of Luya Mountain, China [J]. Chin J Plan Ecolo, 2015, 39(7): 746-752.
[3] FAN Da-Yong,XIONG Gao-Ming,ZHANG Ai-Ying,LIU Xi,XIE Zong-Qiang,LI Zhao-Jia. Effect of water-lever regulation on species selection for ecological restoration practice in the water-level fluctuation zone of Three Gorges Reservoir [J]. Chin J Plan Ecolo, 2015, 39(4): 416-432.
[4] YANG Chun, TAN Tai-Long, YU Jia-Ling, LIAO Qiong, ZHANG Xiao-Long, ZHANG Zhen-Hua, SONG Hai-Xing, and GUAN Chun-Yun. Effects of atmospheric CO2 enrichment on phloem sap composition and root nitrogen accumulation in oilseed rape [J]. Chin J Plan Ecolo, 2014, 38(7): 776-784.
[5] Yu Meng, Ruijuan Gong, Bao Di, Diying Xiang, Gang Zhang, Chengli Xu, Yunfei Li. Electrical Impedance Spectroscopy Estimation of Water Content in Leaves and Stems of White Birch (Betula platyphylla) Under Flooding Stress [J]. Chin Bull Bot, 2014, 49(1): 105-113.
[6] Yujing Wang, Minchun Li, Wang Wu, Hanying Wu, Yinong Xu. Cloning and Characterization of an AP2/EREBP Gene TmAP2-1 from Tetraena mongolica [J]. Chin Bull Bot, 2013, 48(1): 23-33.
[7] YU Li-Min, WANG Chuan-Kuan, and WANG Xing-Chang. Allocation of nonstructural carbohydrates for three temperate tree species in Northeast China [J]. Chin J Plan Ecolo, 2011, 35(12): 1245-1255.
[8] Yuangang Zu;Jing Jia;Wenjie Wang;Fengjian Yang;Huafeng Chen;Naijing Zhang. Changes in Several Physiological-biochemical Parameters During the Life Cycle of Iva xanthifolia [J]. Chin Bull Bot, 2006, 23(4): 348-355.
Full text



[1] Yan Xiao-hua Cai Zhu-ping. Effects of S-07, PP333 and Triadimefon on Peroxidaseisoentyme of Rice Seedling[J]. Chin Bull Bot, 1995, 12(专辑3): 109 -112 .
[2] . [J]. Chin Bull Bot, 1994, 11(专辑): 13 .
[3] Xiaomin Yu;Xingguo Lan;Yuhua Li. The Ub/26S Proteasome Pathway and Self-incompatible Responses in Flowering Plants[J]. Chin Bull Bot, 2006, 23(2): 197 -206 .
[4] Dai Yun-ling and Xu Chun-hui. Advances in Research on Protein Components of Oxygen-evolving Complex[J]. Chin Bull Bot, 1992, 9(03): 1 -16 .
[5] . Advances in Research on Photosynthesis of Submerged Macrophytes[J]. Chin Bull Bot, 2005, 22(增刊): 128 -138 .
[6] Shaobin Zhang;Guoqin Liu. Research Advances in Plant Actin Isoforms[J]. Chin Bull Bot, 2006, 23(3): 242 -248 .
[8] MA Li-Hui, WU Pu-Te, and WANG You-Ke. Spatial pattern of root systems of dense jujube plantation with jujube age in the semiarid loess hilly region of China[J]. Chin J Plan Ecolo, 2012, 36(4): 292 -301 .
[9] PAN Yu-De, Melillo J. M., Kicklighter D. W., XIAO Xiang-Ming, McGuire A. D.. Modeling Structural and Functional Responses of Terrestria Ecosystems in China to Changes in Climate and Atmospheric CO2[J]. Chin J Plan Ecolo, 2001, 25(2): 175 -189 .
[10] . [J]. Chin J Plan Ecolo, 2013, 37(12): 1172 .