Biodiversity Science ›› 2018, Vol. 26 ›› Issue (6): 611-619.doi: 10.17520/biods.2017268

• Original Papers • Previous Article     Next Article

Difference in pH value and nutrient and bacterial diversity in the Carya cathayensis forest soil under different management models

Mei Zhang, Mashui Lin, Xiuxiu Cao, Shumin Zhao, Daqing Jiang, Bingxuan Wang, Shiying Wang, Yandi Fan, Ming Guo, Haiping Lin*()   

  1. Local and National Joint Engineering Laboratory of Biopesticide High-Efficient Preparation, Zhejiang Agriculture and Forestry University, Lin’an, Zhejiang 311300
  • Received:2017-10-11 Accepted:2018-03-08 Online:2018-09-11
  • Lin Haiping E-mail:zjlxylhp@163.com
  • About author:

    # Co-first authors

To optimize management of the Carya cathayensis forest through the diversity and function of soil bacteria, disease index, soil pH, and nutrient and soil bacterial diversity were investigated under ecological management and excessive management during the Botryosphaeria dothidea infected period using 16S rRNA gene high-throughput sequencing technology. The correlations between each interrelationship factors were also analyzed. Results showed that the disease index of the ecologically managed forest was 3.3±3.35, which was significantly lower than that of the excessively managed forest with 81.9±1.27. Moreover, ecological management significantly improved the ability of hickory forest resistant to B. dothidea. The soil pH value of the ecologically managed forest was near neutral with a reading of 6.64±0.06, which was significantly higher than that of excessively managed forest soil with 5.80±0.04. The contents of available phosphorus, available potassium, and available nitrogen in the excessively managed forest soil were 18.10±0.58 mg/kg, 698.63±11.24 mg/kg and 227.13±3.81 mg/kg, which were significantly higher than those in the ecologically managed forest respectively, with 14.94±0.27 mg/kg, 497.13±6.19 mg/kg and 195.28±6.01 mg/kg. There were 14 and 21 major bacterial genera found in the ecologically and excessively managed forest soil samples, respectively. In ecologically managed forest soils, the dominant genera were Sphingomonas, Gaiella and Lysobacter, and the relative abundance of these was significantly higher than excessively managed forest soils. Bryobacter, Candidatus Solibacter, and Bradyrhizobium were the dominant genera in the excessively managed forest soils, and their relative abundance was significantly higher than the ecologically managed forest soils. There was no significant difference of OTUs or Ace, Chao, Shannon and Simpson indices between ecologically and excessively managed forest soils. Redundancy analysis (RDA) and Monte Carlo testing showed that pH value, available phosphorous and available nitrogen had significant effects on the bacterial flora of the dominant bacterial species in the soil (P < 0.05). Our results can provide valuable references for the sustainable management of hickory forests.

Key words: ecological management, excessive management, Carya cathayensis canker disease, bacterial diversity, pH value, soil nutrient

Table 1

The comparison of pH value, nutrient contents and bacterial diversity indices of hickory forest under different management models"

指标
Item
生态经营
Ecological
management
过度经营
Excessive
management
pH 6.64 ± 0.06 a 5.80 ± 0.04 b
速效磷 AP (mg/kg) 14.94 ± 0.27 b 18.10 ± 0.58 a
速效钾 AK (mg/kg) 497.13 ± 6.19 b 698.63 ± 11.24 a
速效氮 AN (mg/kg) 195.28 ± 6.01 b 227.13 ± 3.81 a
有机碳 OC (g/kg) 36.27 ± 1.58 a 37.57 ± 6.13 a
OTUs 3,786 ± 82 a 3,569 ± 128 a
Ace指数 Ace index 4,198 ± 136.80 a 4,044 ± 320.22 a
Chao指数 Chao index 4,117 ± 152.61 a 4,032 ± 304.55 a
Shannon指数 Shannon index 9.861 ± 0.116 a 9.648 ± 0.079 a
Simpson指数 Simpson index 0.9969 ± 0.0003 a 0.9965 ± 0.0003 a

Fig. 1

Species relative abundance clustering heatmap of bacteria of hickory forest soil under different management models. The corresponding values in heatmap are Z values which are obtained after standardized treatment of the relative abundance of each row of the species."

Table 2

The differences of dominant bacterial flora and relative abundance of hickory forest soil under different management models"

菌群
Bacterial flora
生态经营 Ecological management (%) 过度经营Excessive management (%)
Sphingomonas 2.29 ± 0.18 a 1.47 ± 0.27 b
Gaiella 0.61 ± 0.07 a 0.41 ± 0.06 b
Lysobacter 0.57 ± 0.10 a 0.26 ± 0.05 b
Bryobacter 0.80 ± 0.08 b 1.03 ± 0.03 a
Candidatus Solibacter 0.87 ± 0.02 b 1.40 ± 0.07 a
Bradyrhizobium 0.67 ± 0.09 b 0.95 ± 0.07 a

Fig. 2

Correlation of the dominant bacterial flora between the genus level and environmental variables of hickory forest soil under different management models. AN, Available nitrogen; AP, Available phosphorus; AK, Available potassium; OC, Organic carbon."

[1] Adhikari TB, Joseph CM, Yang G, Phillips DA, Nelson LM (2001) Evaluation of bacteria isolated from rice for plant growth promotion and biological control of seedling disease of rice. Canadian Journal of Microbiology, 47, 916-924.
[2] Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK (2010) QIIME allows analysis of high-throughput community sequencing data. Nature methods, 7, 335-336.
[3] Chen PP, Guo LL, Tang LZ, Lu HY, Yuan ZG, Yang J, Yi ZX, Tu NM (2017) Effect of soil pH on nitrogen utilization efficiency and biological characters of rhizosphere soil of rice varieties with different acid-sensitivity. Journal of Nuclear Agricultural Sciences, 31, 757-767. (in Chinese with English abstract)
[陈平平, 郭莉莉, 唐利忠, 卢浩宇, 袁珍贵, 杨晶, 易镇邪, 屠乃美 (2017) 土壤pH对不同酸性敏感型水稻品种氮利用效率与根际土壤生物学特性的影响. 核农学报, 31, 757-767.]
[4] Chen SQ (2012) Study on the Nutrient Diagnosis and Ecological Management of the Carya cathayensis Plantation. PhD dissertation, Nanjing Forestry University, Nanjing. (in Chinese with English abstract)
[陈世权 (2012) 山核桃人工林养分诊断及生态经营技术研究. 博士学位论文, 南京林业大学, 南京.]
[5] Chen W, Ouyang LM, Kong PJ, Yang ZY, Wu W, Zhu DL, Zhang LL (2015) Rhizospheria bacteria of Populus euphratica improve resistance of wood plants to heavymetals. Chinese Journal of Applied Ecology, 26, 2811-2816. (in Chinese with English abstract)
[陈雯, 欧阳立明, 孔沛筠, 杨泽宇, 吴蔚, 朱冬林, 张利莉 (2015) 胡杨根际细菌提高木本植物对重金属胁迫的耐受性. 应用生态学报, 26, 2811-2816.]
[6] Christensen P, Cook FD (1978) Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. International Journal of Systematic Bacteriology, 28, 367-393.
[7] Dai DJ, Ma HQ, Shen Y, Zhang CQ, Wang HD (2015) Application and screening of fungicides for controlling carya tree canker caused by Botryosphaeria dothidea. Agrochemicals, 54, 217-230. (in Chinese with English abstract)
[戴德江, 马海芹, 沈瑶, 张传清, 王华弟 (2015) 几种杀菌剂对山核桃干腐病的室内活性筛选与应用. 农药, 54, 217-230.]
[8] Deng WQ, Liu SL, Yao K, Li JL, Han XF, Liang JF, Wang ZL, Luo PW, Jia QS (2015) Study on the influence of environmental conditions and intermediates of phenol degradation by a 3-phenoxybenzoic acid degrading strain Sphingomonas sp. SC-1. Microbiology China, 42, 497-503. (in Chinese with English abstract)
[邓维琴, 刘书亮, 姚开, 李建龙, 韩新锋, 梁金凤, 王志龙, 罗佩文, 贾秋思 (2015) 3-苯氧基苯甲酸降解菌Sphingomonas sp. SC-1降解苯酚环境条件及其降解中间产物的研究. 微生物学通报, 42, 497-503.]
[9] Edgar RC (2013) UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996-998.
[10] Gao SC, Guan DW, Ma MC, Zhang W, Li J, Shen DL (2017) Effects of fertilization on bacterial community under the condition of continuous soybean monoculture in black soil in Northeast China. Scientia Agricultura Sinica, 50, 1271-1281. (in Chinese with English abstract)
[高圣超, 关大伟, 马鸣超, 张伟, 李俊, 沈德龙 (2017) 大豆连作条件下施肥对东北黑土细菌群落的影响. 中国农业科学, 50, 1271-1281.]
[11] Gou M, Qu YY, Yang H, Zhou JT, Li A, Guan XY, Ai FF (2008) Sphingomonas sp.: A novel microbial resource for biodegradation of aromatic compounds. Chinese Journal of Applied and Environmental Biology, 14, 276-282. (in Chinese with English abstract)
[苟敏, 曲媛媛, 杨桦, 周集体, 李昂, 关晓燕, 艾芳芳 (2008) 鞘氨醇单胞菌: 降解芳香化合物的新型微生物资源. 应用与环境生物学报, 14, 276-282.]
[12] Han WY, Wang WM, Guo Y, Yang MZ, Jia ZJ (2013) Bacterial Abundance of Tea Garden Soils and Its Influencing Factors. Journal of Tea Science, 33, 147-154. (in Chinese with English abstract)
[韩文炎, 王皖蒙, 郭赟, 杨明臻, 贾仲君 (2013) 茶园土壤细菌丰度及其影响因子研究. 茶叶科学, 33, 147-154.]
[13] Ji GH (2011) Advances in the study on Lysobacter spp. bacteria and their effects on biological control of plant Diseases. Journal of Yunnan Agricultural University (Natural Science), 26, 124-130. (in Chinese with English abstract)
[姬广海 (2011) 溶杆菌属及其在植物病害防治中的研究进展. 云南农业大学学报(自然科学), 26, 124-130.]
[14] Ju YW, Zhao PP, Huang L, Cao X, Liang Y, Ye J, Gao J (2015) Analysis of Carya illinoensis main diseases occurrence and control. Journal of Nanjing Forestry University, 39(4), 31-36. (in Chinese with English abstract)
[巨云为, 赵盼盼, 黄麟, 曹霞, 梁艳, 叶健, 高瑾 (2015) 薄壳山核桃主要病害发生规律及防控. 南京林业大学学报, 39(4), 31-36.]
[15] Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung HY, Lee IJ (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. Journal of Microbiology, 52, 689-695.
[16] Li S, Jochum CC, Yu F, Zaletarivera K, Du L, Harris SD, Yuen GY (2008) An antibiotic complex from Lysobacter enzymogenes strain C3: Antimicrobial activity and role in plant disease control. Phytopathology, 98, 695-701.
[17] Lu HF, Zheng JW, Yu XC, Zhou HM, Zheng JF, Zhang XH, Liu XY, Cheng K, Li LQ, Pan GX (2015) Microbial community diversity and enzyme activity of red paddy soil under long-term combined inorganic-organic fertilization. Journal of Plant Nutrition and Fertilizer, 21, 632-643. (in Chinese with English abstract)
[陆海飞, 郑金伟, 余喜初, 周惠民, 郑聚锋, 张旭辉, 刘晓雨, 程琨, 李恋卿, 潘根兴 (2015) 长期无机有机肥配施对红壤性水稻土微生物群落多样性及酶活性的影响. 植物营养与肥料学报, 21, 632-643.]
[18] Lv QJ, Shen YQ, Gao YL, Huang JQ (2012) Development process, agents and prospect of hickory industry. Zhejiang Province. Journal of Zhejiang A & F University, 29, 97-103. (in Chinese with English abstract)
[吕秋菊, 沈月琴, 高宇列, 黄坚钦 (2012) 山核桃产业的发展过程、动因及展望. 浙江农林大学学报, 29, 97-103.]
[19] Nanjing Institute of Soil Science, Chinese Academy of Sciences(1978) Soil Physical and Chemical Analysis. Shanghai Science and Technology Press, Shanghai. (in Chinese)
[中国科学院南京土壤研究所(1978) 土壤理化分析. 上海科学技术出版社, 上海.]
[20] Qian JF, Wu JS, Huang JQ (2014) Effects of sod-cultural practices on soil nutrients and microbial diversity in the Carya cathayensis forest. Acta Ecologica Sinica, 34, 4324-4332. (in Chinese with English abstract)
[钱进芳, 吴家森, 黄坚钦 (2014) 生草栽培对山核桃林地土壤养分及微生物多样性的影响. 生态学报, 34, 4324-4332.]
[21] Ren HS, Xu WF, Wang AY, Zuo WD, Xie J (2017) Research on biodiversity of endophytic bacteria and the antagonistic endophytes in mulberry. Journal of Southwest University (Natural Science Edition), 39, 36-45. (in Chinese with English abstract)
[任慧爽, 徐伟芳, 王爱印, 左伟东, 谢洁 (2017) 桑树内生细菌多样性及内生拮抗活性菌群的研究. 西南大学学报(自然科学版), 39, 36-45.]
[22] Shen YF, Qian JF, Zheng XP, Yuan ZQ, Huang JQ, Wen GS, Wu JS (2016) Spatial-temporal variation of soil fertility in Chinese walnut (Carya cathayensis) plantation. Science Silvae Sinicae, 52(7), 1-12. (in Chinese with English abstract)
[沈一凡, 钱进芳, 郑小平, 袁紫倩, 黄坚钦, 温国胜, 吴家森 (2016) 山核桃中心产区林地土壤肥力的时空变化特征. 林业科学, 52(7), 1-12.]
[23] Shen YQ, Zhu Z, Wu WG, Gao YL, Lin JH, Huang JQ (2010) Farmers' willingness to management way of non-wood forest products and its influencing factors. Journal of Nature Resources, 25, 192-199. (in Chinese with English abstract)
[沈月琴, 朱臻, 吴伟光, 高宇列, 林建华, 黄坚钦 (2010) 农户对非木质林产品经营模式的选择意愿及其影响因素分析. 自然资源学报, 25, 192-199.]
[24] Song ZQ, Wang L, Liu XH, Liang F (2016) The diversities of Proteobacteria in four acidic hot springs in Yunnan. Journal of Henan Agricultural University, 50, 376-382. (in Chinese with English abstract)
[宋兆齐, 王莉, 刘秀花, 梁峰 (2016) 云南4处酸性热泉中的变形菌门细菌多样性. 河南农业大学学报, 50, 376-382.]
[25] Wang J, Song Y, Ma T, Raza W, Li J, Howland JG, Huang Q (2017) Impacts of inorganic and organic fertilization treatments on bacterial and fungal communities in a paddy soil. Applied Soil Ecology, 112, 42-50.
[26] Wu JS, Qian JF, Tong ZP, Huang JQ, Zhao KL (2014) Changes in soil organic carbon and soil microbial functional diversity of Carya cathayensis plantations under intensive managements. Chinese Journal of Applied Ecology, 25, 2486-2492. (in Chinese with English abstract)
[吴家森, 钱进芳, 童志鹏, 黄坚钦, 赵科理 (2014) 山核桃林集约经营过程中土壤有机碳和微生物功能多样性的变化. 应用生态学报, 25, 2486-2492.]
[27] Xue C (2015) Manipulation of Microbial Community in Banana Rhizospherer to Suppress Fusarium Wilt of Banana. PhD dissertation, Nanjing Agricultural University, Nanjing. (in Chinese with English abstract)
[薛超 (2015) 香蕉根际土壤微生物区系特征与土传枯萎病防控研究. 博士学位论文, 南京农业大学, 南京.]
[28] Yang SZ, Ding LZ, Lou JF, Zhang QY, Wu JL, Hu GL (2009) Occurrence regularity of Carya cathayensis canker disease and its control. Journal of Zhejiang Forestry College, 26, 228-232. (in Chinese with English abstract)
[杨淑贞, 丁立忠, 楼君芳, 张秋月, 吴继来, 胡国良 (2009) 山核桃干腐病发生发展规律及防治技术. 浙江林学院学报, 26, 228-232.]
[29] Yu H (2015) Regulation Effect of Straw Returning Mode into Field on Soil Microorganism and Growth Properties in Maize. PhD dissertation, Jilin Agricultural University, Changchun. (in Chinese with English abstract)
[于寒 (2015) 秸秆还田方式对土壤微生物及玉米生长特性的调控效应研究. 博士学位论文, 吉林农业大学, 长春.]
[30] Yu L, Chen J, Chen LJ, Cheng JB, Wu JS, Xia GH (2011) Effect of interplantation of green manure varieties on yield of hickey forests. Journal of Forestry Engineering, 25(3), 92-95. (in Chinese with English abstract)
[余琳, 陈军, 陈丽娟, 程建斌, 吴家森, 夏国华 (2011) 山核桃投产林林下套种绿肥效应. 林业工程学报, 25(3), 92-95.]
[31] Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnology and Bioengineering, 89, 670-679.
[32] Zhang LH, Wang YJ, Liao L, Ji GH (2011) Biocontrol effect of Lysobacter antibioticus 06-4 on soft rot pathogen of Amorphophallus konjac its mechanism. Journal of Hunan Agricultural University, 37, 286-289. (in Chinese with English abstract)
[张丽辉, 王永吉, 廖林, 姬广海 (2011) 生防菌06-4对魔芋软腐病的防治及机理的初步研究. 湖南农业大学学报, 37, 286-289.]
[33] Zhang LL, Jia GM, Ye JF, Ma LJ (2013) Frequency of Carya cathayensis canker disease in Lin’an City, Zhejiang Province. Journal of Zhejiang A & F University, 30, 148-152. (in Chinese with English abstract)
[张璐璐, 贾桂民, 叶建丰, 马良进 (2013) 浙江临安山核桃干腐病发生发展规律. 浙江农林大学学报, 30, 148-152.]
[34] Zhang ZY, Tang JX, Wang SF, Wang QL (2009) Effects of N, P, K on growth and development of plants and its physiological mechanisms. Guangdong Agricultural Sciences, 36(5), 89-92. (in Chinese with English abstract)
[张志勇, 汤菊香, 王素芳, 王清连 (2009) 氮磷钾对植物侧根生长发育的影响及其生理机制. 广东农业科学, 36(5), 89-92.]
[35] Zheng WJ (1985) Sylva Sinica (2). China Forestry Publishing House, Beijing. (in Chinese)
[郑万钧 (1985) 中国树木志(2). 中国林业出版社, 北京.]
[36] Zhou J, Lei T (2007) Review and prospects on methodology and affecting factors of soil microbial diversity. Biodiversity Science, 15, 306-311. (in Chinese with English abstract)
[周桔, 雷霆 (2007) 土壤微生物多样性影响因素及研究方法的现状与展望. 生物多样性, 15, 306-311.]
[1] GOU Xiao-Lin, ZHOU Qing-Ping, CHEN You-Jun, WEI Xiao-Xing, TU Wei-Guo. Characteristics of nutrients in two dominant plant species and rhizospheric soils in alpine desert of the Qinghai-Xizang Plateau under contrasting climates [J]. Chin J Plan Ecolo, 2018, 42(1): 133-142.
[2] Rui-Yu ZHAO, Zheng-Cai LI, Bin WANG, Xiao-Gai GE, Yun-Xi DAI, Zhi-Xia ZHAO, Yu-Jie ZHANG. Duration of mulching caused variable pools of labile organic carbon in a Phyllostachys edulis plantation [J]. Chin J Plan Ecolo, 2017, 41(4): 418-429.
[3] Jing Yan,Xiaoya Zhang,Xue Chen,Yue Wang,Fengjuan Zhang,Fanghao Wan. Effects of rhizosphere soil microorganisms and soil nutrients on competitiveness of Bidens pilosa with different native plants [J]. Biodiv Sci, 2016, 24(12): 1381-1389.
[4] Dan LI, Saruul KANG, Meng-Ying ZHAO, Qing ZHANG, Hai-Juan REN, Jing REN, Jun-Mei ZHOU, Zhen WANG, Ren-Ji WU, Jian-Ming NIU. Relationships between soil nutrients and plant functional traits in different degradation stages of Leymus chinensis steppe in Nei Mongol, China [J]. Chin J Plan Ecolo, 2016, 40(10): 991-1002.
[5] XU Ming-Shan,ZHAO Yan-Tao,YANG Xiao-Dong,SHI Qing-Ru,ZHOU Liu-Li,ZHANG Qing-Qing,Ali ARSHAD,YAN En-Rong. Geostatistical analysis of spatial variations in leaf traits of woody plants in Tiantong, Zhejiang Province [J]. Chin J Plan Ecolo, 2016, 40(1): 48-59.
[6] TANG Hai-Ping,CHEN Jiao,XUE Hai-Li. Ecological thresholds: Concept, Methods and research outlooks [J]. Chin J Plan Ecolo, 2015, 39(9): 932-940.
[7] Aihua Zhao,Xiaojun Du,Jing Zang,Shouren Zhang,Zhihua Jiao. Soil bacterial diversity in the Baotianman deciduous broad-leaved forest [J]. Biodiv Sci, 2015, 23(5): 649-657.
[8] MA Yu-Zhu,ZHONG Quan-Lin,JIN Bing-Jie,LU Hong-Dian,GUO Bing-Qiao,ZHENG Yuan,LI Man,CHENG Dong-Liang. Spatial changes and influencing factors of fine root carbon, nitrogen and phosphorus stoichiometry of plants in China [J]. Chin J Plan Ecolo, 2015, 39(2): 159-166.
[9] ZHANG Cui-Ping, MENG Ping, LI Jian-Zhong, WAN Xian-Chong. Interactive effects of soil acidification and phosphorus deficiency on photosynthetic characteristics and growth in Juglans regia seedlings [J]. Chin J Plan Ecolo, 2014, 38(12): 1345-1355.
[10] LIU Jun, YANG Qing-Pei, YU Ding-Kun, SONG Qing-Ni, ZHAO Guang-Dong, and WANG Bing. Contribution of fine root to soil nutrient heterogeneity at two sides of the bamboo and broadleaved forest interface [J]. Chin J Plan Ecolo, 2013, 37(8): 739-749.
[11] DI Nan, XI Ben-Ye, Jeremiah R. PINTO, WANG Ye, LI Guang-De, and JIA Li-Ming. Root biomass distribution of triploid Populus tomentosa under wide- and narrow-row spacing planting schemes and its responses to soil nutrients [J]. Chin J Plan Ecolo, 2013, 37(10): 961-971.
[12] TU Li-Hua, HU Ting-Xing, ZHANG Jian, LI Ren-Hong, DAI Hong-Zhong, LUO Shou-Hua. Response of soil organic carbon and nutrients to simulated nitrogen deposition in Pleioblastus amarus plantation, Rainy Area of West China [J]. Chin J Plan Ecolo, 2011, 35(2): 125-136.
[13] ZHANG Gui-Ling. Effects of straw and living grass mulching on soil nutrients, soil microbial quantities and soil enzyme activities in a peach orchard [J]. Chin J Plan Ecolo, 2011, 35(12): 1236-1244.
[14] ZHANG Zhong-Hua, HU Gang, ZHU Jie-Dong, and NI Jian. Spatial heterogeneity of soil nutrients and its impact on tree species distribution in a karst forest of Southwest China [J]. Chin J Plan Ecolo, 2011, 35(10): 1038-1049.
[15] YUAN Li-Huan, YAN Gui-Qin. Rhizospheric soil of seedlings of Elaeagnus mollis colonized by arbuscular mycorrhizal fungi [J]. Chin J Plan Ecolo, 2010, 34(6): 678-686.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Kao Tso-Ching, Cheng Ching-Yung. New Taxa of the Chinese Celastraceae (1)[J]. J Syst Evol, 1988, 26(4): 310 -314 .
[2] CHANG Sheng-He, YING Jia, ZHANG Ji-Jun, LI Bin, LI Zhen-Sheng. Isolation and Characterization of a BBC1 cDNA from Common Wheat[J]. J Integr Plant Biol, 2003, 45(7): 878 -882 .
[3] . [J]. Chin J Plan Ecolo, 2015, 39(11): 1123 .
[4] Yin Shu-Fen. New Taxa of Fritillaria from Anhui Province[J]. J Syst Evol, 1983, 21(1): 100 -101 .
[5] Guijun Yang, Wenjiang Huang, Jihua Wang, Zhurong Xing. Inversion of Forest Leaf Area Index Calculated from Multi-source and Multi-angle Remote Sensing Data[J]. Chin Bull Bot, 2010, 45(05): 566 -578 .
[6] Ke-Fu Zhao, Jie Song, Hai Fan, San Zhou, and Meng Zhao. Growth Response to Ionic and Osmotic Stress of NaCl in Salt-tolerant and Salt-sensitive Maize[J]. J Integr Plant Biol, 2010, 52(5): 468 -475 .
[7] . [J]. Chin J Plan Ecolo, 1964, (2): 265 .
[8] Pengtao Wang, Jing Zhao, Huanhuan Yu. Reactive Oxygen Species Signaling in Stomata[J]. Chin Bull Bot, 2014, 49(4): 490 -503 .
[9] Tao Yan, Tiantian Qu, Huanhuan Song, Philippe Ciais, Shilong Piao, Zhenzhong Sun and Hui Zeng. Contrasting effects of N addition on the N and P status of understory vegetation in plantations of sapling and mature Larix principis-rupprechtii[J]. J Plant Ecol, 2018, 11(6): 843 -852 .
[10] CUI Xiao-Yong, Du Zhan-Chi, Wang Yan-Fen. Photosynthetic Characteristics of a Semi-arid Sandy Grassland Community in Inner Mongolia[J]. Chin J Plan Ecolo, 2000, 24(5): 541 -546 .