Chinese Journal of Plant Ecology >
Research Articles
Effects of solid culture endophytic fungi on osmotic adjustment and antioxidant system of Casuarina equisetifolia seedlings under soil salt stress
Expand
- 1College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China
2The Higher Educational Key Laboratory for Forest Ecosystem Process and Management of Fujian Province, Fuzhou 350002, China
3Fujian Hui’an Chihu State-owned Forest Shelter Farm, Hui’an, Fujian 362100, China
Received date: 2022-02-14
Accepted date: 2022-05-21
Online published: 2022-06-09
Supported by
National Natural Science Foundation of China(32071753)
Abstract
Aims Endophyte is a new microbial resource, which has a complex micro-ecological relationship with plants. In this paper, the antagonistic effect of endophytic fungi on the growth of salt-tolerant plants was confirmed by adding endophytic fungi to the plants and testing the physiological characteristics and biomass of the seedlings.
Methods Two salt-tolerant endophytic fungi Botryosphaeria sp. Z1 (T3), Hypoxylon sp. Y6 (T4), and their mixture (T2) were cultured in solid fermentation and added to potted soil planted with seedlings of Casuarina equisetifolia at different salinity (mass fraction: 0, 3‰, 6‰ and 9‰), which were treated with an added fungi of seedlings. The addition of microbiological medium (T1) and no added microbiological medium (CK) were treated as two experimental controls, which was to confirm the effect of the fungi, but not the microbiological medium. Samples were taken at 15 day intervals, four times, for a total of 60 days, and the relative electronic conductivity (REC), malondialdehyde (MDA) content, soluble sugar (SS) content, soluble protein (SP) content, proline (PRO) content, superoxide dismutase (SOD) activity, peroxidase (POD) activity, catalase (CAT) activity, reactive oxygen (H2O2) content of leaves and the biomass of seedling were determined each time.
Important findings We found that the biomass of seedlings treated by fungal strain was significantly increased under salt stress, and the physiological characteristics were significantly affected by soil salinity, time and fungal species. At 3‰ salinity, the contents of SS and SP, and the activity of SOD and CAT were higher in T2 treatment than in CK and T1 after 15 days of treatment, but the REC was significantly lower in T2, T3 and T4 treatments during the stress period. At 9‰ salinity, T2 treatment significantly reduced the REC and the contents of H2O2 and MDA, but significantly increased the content of SS and the activity of SOD and CAT. Especially, SP content and POD activity were also significantly increased in T2 treatment after 60 days. A stepwise regression was used to model the relationship between physiological characteristics and biomass of seedlings treated with the strains, and the path analysis showed that REC, POD activity and SS content were the main physiological factors affecting biomass. In conclusion, the effects of different fungi on the content of osmoregulatory substances, oxidase activity and biomass of seedlings were different, and the antagonistic effect of the mixed fungi was the most obviously. Thus, the relationship between osmotic regulatory substances, antioxidant enzymes, biomass and endophytic fungi of C. equisetifolia under salt stress was clarified, which provided a basic for the further study on the stress resistant engineering fungi for C. equisetifolia.
Cite this article
LI Guan-Jun, CHEN Long, YU Wen-Jing, SU Qin-Gui, WU Cheng-Zhen, SU Jun, LI Jian . Effects of solid culture endophytic fungi on osmotic adjustment and antioxidant system of Casuarina equisetifolia seedlings under soil salt stress[J]. Chinese Journal of Plant Ecology, 2023 , 47(6) : 804 -821 . DOI: 10.17521/cjpe.2022.0061
References
| [1] | Arnold AE (2007). Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biology Reviews, 21, 51-66. |
| [2] | Chen TT (2008). Water Use Efficiency and Response to Light of Several Shrubs in Different Water Moisture in Datong Town in Qinghai. Master degree dissertation, Beijing Forestry University, Beijing. 50-52. |
| [2] | [陈婷婷 (2008). 青海省大通县常见灌木不同水分条件下水分利用效率及光响应研究. 硕士学位论文, 北京林业大学, 北京. 50-52.] |
| [3] | Chen YF (2017). The Main Problem of Vegetation Restoration in the Coastal Areas of South China—Salt Spray Injury. Master degree dissertation, Xiamen University, Xiamen, Fujian. 26-28. |
| [3] | 陈洋芳 (2017). 我国南方滨海地区植被修复的主要难题——盐雾危害. 硕士学位论文, 厦门大学, 福建厦门. 26-28.] |
| [4] | Chen ZH, Wu L, Yang QM, Wang JY, Zhu MJ, Du XP (2013). Isolation and identification of endophytic fungi from mangrove plants and screening of antibacterial active strains. Acta Laser Biology Sinica, 22, 263-266. |
| [4] | [陈昭华, 伍菱, 杨秋明, 王骥妍, 朱敏佳, 杜希萍 (2013). 红树植物内生真菌的分离鉴定及抗菌活性菌株的筛选. 激光生物学报, 22, 263-266.] |
| [5] | Du WY, Wang M, Yan ZB, Wang JF, Chen XS, Shen X, Yin CM, Mao ZQ (2020). Effects of residual apple fermentation products on continuous cropping soil environment and the growth of Malus hupehensis Rehd. seedlings. Chinese Journal of Applied Ecology, 31, 1443-1450. |
| [5] | [杜文艳, 王玫, 闫助冰, 王建锋, 陈学森, 沈向, 尹承苗, 毛志泉 (2020). 残次苹果发酵产物对连作土壤环境及‘平邑甜茶’幼苗生长的影响. 应用生态学报, 31, 1443-1450.] |
| [6] | Feng L, Song FQ (2011). The impacts of combination of ectomycorrhizal fungi with filamentous fungi on decomposition of Korean-pine litterfall. Ecological Science, 30, 315-320. |
| [6] | [冯乐, 宋福强 (2011). 外生菌根真菌与丝状真菌混合对红松凋落物降解效能的影响. 生态科学, 30, 315-320.] |
| [7] | Gao HY (2009). Research on the Inhibiting Substances of Hypoxylon Perforatum and Their Effects on Sphaeropsis sapinea. Master degree dissertation, Northeast Forestry University, Harbin. 33-35. |
| [7] | [高海燕 (2009). 炭团菌抑菌活性成分及其对松枯梢病菌的影响. 硕士学位论文, 东北林业大学, 哈尔滨. 33-35.] |
| [8] | Gao Y, Cao F, Li H, Liu SP, Xue YH (2019). Antioxidant of coumarin analogues from endophytic Aspergillus fumigatus in riparian zone to improve anti-waterlogging ability in Arabidopsis thaliana. Journal of Microbiology, 39(6), 56-64. |
| [8] | [高媛, 曹飞, 李辉, 刘士平, 薛艳红 (2019). 河岸带内生烟曲霉的香豆素类抗氧化产物提高拟南芥抗涝害能力研究. 微生物学杂志, 39(6), 56-64.] |
| [9] | Hallasgo AM, Spangl B, Steinkellner S, Hage-Ahmed K (2020). The fungal endophyte Serendipita williamsii does not affect phosphorus status but carbon and nitrogen dynamics in arbuscular mycorrhizal tomato plants. Journal of Fungi, 6, 233. DOI: 10.3390/jof6040233. |
| [10] | He HQ, Peng XY, Tao S, Wang YN, Xu Y, Lin JX (2019). Effects of arbuscular mycorrhizal fungi on growth and antioxidant enzyme activities of Leymus chinensis seedlings under salt (alkali) and drought stress. Modern Agricultural Science and Technology, (12), 149-150. |
| [10] | [何汉琼, 彭晓媛, 陶爽, 王英男, 徐瑶, 蔺吉祥 (2019). 丛枝菌根真菌对盐(碱)-旱交叉胁迫下羊草幼苗生长与抗氧化酶活性的影响. 现代农业科技, (12), 149-150.] |
| [11] | Holguin G, Bashan Y (1996). Nitrogen-fixation by Azospirillum brasilense Cd is promoted when co-cultured with a mangrove rhizosphere bacterium (Staphylococcus sp.). Soil Biology & Biochemistry, 28, 1651-1660. |
| [12] | Huang HG, Lü LX, Zhang YM, Jiang Z, Shen Y, An QL (2017). Microbe-assisted drought resistance for tobacco plants: mechanisms and applications. Chinese Journal of Applied Ecology, 28, 3099-3110. |
| [12] | [黄化刚, 吕立新, 张艳茗, 姜壮, 申燕, 安千里 (2017). 微生物帮助烟草抗旱的机理及其应用. 应用生态学报, 28, 3099-3110.] |
| [13] | Ji YH (2005). Research of the seedling salt-tolerance of new poplar and willow clones on the seashore marsh. Journal of Jiangsu Forestry Science & Technology, (4), 1-4. |
| [13] | [季永华 (2005). 海滨湿地杨树、柳树新无性系苗期耐盐性研究. 江苏林业科技, (4), 1-4.] |
| [14] | Jiang D, Lu B, Liu LT, Duan WJ, Chen L, Li J, Zhang K, Sun HC, Zhang YJ, Dong HZ, Li CD, Bai ZY (2020). Exogenous melatonin improves salt stress adaptation of cotton seedlings by regulating active oxygen metabolism. PeerJ, 8, e10486. DOI: 10.7717/peerj.10486. |
| [15] | Kong P, Hong CX (2020). Endophytic Burkholderia sp. SSG as a potential biofertilizer promoting boxwood growth. PeerJ, 8, e9547. DOI: 10.7717/peerj.9547. |
| [16] | Kumar A, Tripti, Voropaeva O, Maleva M, Panikovskaya K, Borisova G, Rajkumar M, Bruno LB (2021). Bioaugmentation with copper tolerant endophyte Pseudomonas lurida strain EOO26 for improved plant growth and copper phytoremediation by Helianthus annuus. Chemosphere, 266, 128983. DOI: 10.1016/j.chemosphere.2020.128983. |
| [17] | Lai XL, Yan YJ, Yan LH (2020). Effects of NaCl stress on growth and physiological characteristics of Dalbergia hupeana seedlings. Plant Physiology Journal, 56, 309-316. |
| [17] | [赖小连, 颜玉娟, 颜立红 (2020). NaCl胁迫对黄檀幼苗生长及生理特性的影响. 植物生理学报, 56, 309-316.] |
| [18] | Li BB, Ouyang J, Wang JY, Wu HF, Liu XJ, Zou JH (2017). Effects of NaCl on seedling growth and some physiological characteristics of Salix matsudana Koidz. Journal of Tianjin Normal University (Natural Science Edition), 37(6), 37-42. |
| [18] | [李斌彬, 欧阳洁, 王嘉玥, 吴航枫, 刘祥君, 邹金华 (2017). NaCl对旱柳生长发育及部分生理特性的影响. 天津师范大学学报(自然科学版), 37(6), 37-42.] |
| [19] | Li GJ, Liang AJ, Yao CS, Lin YM, Li J (2022). Effect of salt stress on the secondary metabolites of endophytic fungi of Casuarina equisetifolia in solid culture. Chinese Journal of Applied and Environmental Biology, 28, 135-142. |
| [19] | [李冠军, 梁安洁, 姚成硕, 林勇明, 李键 (2022). 盐胁迫对木麻黄内生真菌固体培养次生代谢产物的影响. 应用与环境生物学报, 28, 135-142.] |
| [20] | Li GJ, Liu XM, Liang AJ, Lin YM, Li J (2019). Effects of NaCl stress on metabolites of two endophytic fungi of Casuarina equisetifolia. Chinese Journal of Applied and Environmental Biology, 25, 902-908. |
| [20] | [李冠军, 刘鑫铭, 梁安洁, 林勇明, 李键 (2019). 两株木麻黄内生真菌代谢产物对NaCl胁迫的响应. 应用与环境生物学报, 25, 902-908.] |
| [21] | Li J, Xie HH, Liu Y, Hong T, Lin YM, Lin H, Chen C, Wu CZ, Hong W (2012). Effect of two allelochemicals of Casuarina equisetifolia on dynamic change of root activity and endogenous hormone of its seedling under hydroponic cultivation. Chinese Journal of Tropical Crops, 33, 2091-2097. |
| [21] | [李键, 谢海慧, 刘奕, 洪滔, 林勇明, 林晗, 陈灿, 吴承祯, 洪伟 (2012). 两种木麻黄化感物质对其水培幼苗根系活力及内源激素含量的动态影响. 热带作物学报, 33, 2091-2097.] |
| [22] | Li J, Zhang BL, Zhao Y, Xin SG, Chen Q, Song NN, Li XM (2014). Progress in endophyte improving plant salt and alkali resistance. Biotechnology Bulletin, (4), 14-18. |
| [22] | [李娇, 张宝龙, 赵颖, 辛士刚, 陈强, 宋宁宁, 李雪梅 (2014). 内生菌对提高植物抗盐碱性的研究进展. 生物技术通报, (4), 14-18.] |
| [23] | Li Q, Yao T, Yang XM, Zhang JG, Feng Y (2020). Effects of different dosages of microbial fertilizers on growth and quality of oat in semi-arid area. Journal of Arid Land Resources and Environment, 34(3), 159-165. |
| [23] | [李琦, 姚拓, 杨晓玫, 张建贵, 冯影 (2020). 半干旱地区不同剂型微生物菌肥替代部分化肥对燕麦生长和品质的影响. 干旱区资源与环境, 34(3), 159-165.] |
| [24] | Liao QL (2012). Influence of soil salinity on growth and physiological indexes of Phoenix canariensis seedlings. Journal of Tropical and Subtropical Botany, 20, 163-168. |
| [24] | [廖启炓 (2012). 土壤盐度对加拿利海枣幼苗生长与生理指标的影响. 热带亚热带植物学报, 20, 163-168.] |
| [25] | Lin H, Hong CJ, Hong T, Xie AQ, Fan HL, Chen XF, Wu CZ (2016). The effect of various endophytic fungi on the growth and main element contents of Aleurites montana seedlings. Chinese Journal of Tropical Crops, 37, 1799-1804. |
| [25] | [林晗, 洪陈洁, 洪滔, 谢安强, 范海兰, 陈欣凡, 吴承祯 (2016). 不同内生真菌对千年桐幼苗生长及主要矿质元素的影响. 热带作物学报, 37, 1799-1804.] |
| [26] | Liu LY, Liu KX, Chi XL, Zhang X, Xu C, Zhu H, Jin X, Liu WW, Sun ZT, Mao ZQ (2018). Effects of bioorganic fertilizer SNB-86 special for continuous cropping apple on Malus hupehensis seedlings and soil environment under replant disease condition. Acta Horticulturae Sinica, 45, 2008-2018. |
| [26] | [刘丽英, 刘珂欣, 迟晓丽, 张潇, 许超, 朱浩, 金晓, 刘维维, 孙中涛, 毛志泉 (2018). 枯草芽孢杆菌SNB-86菌肥对连作平邑甜茶幼苗生长及土壤环境的影响. 园艺学报, 45, 2008-2018.] |
| [27] | Long F (2018). Regulation of Endophytic Fungi on Physiological Characteristics of Casuarina equisetifolia Seedlings Under NaCl Stress. Master degree dissertation, Fujian Agriculture and Forestry University, Fuzhou. 56-58. |
| [27] | 龙凤 (2018). 内生真菌对NaCl胁迫下短枝木麻黄幼苗生理特征的调控研究. 硕士学位论文, 福建农林大学, 福州. 56-58.] |
| [28] | Lü R, Yao Y, Duan RJ, Li RM, Liu J, Fu SP, Hu XW, Guo JC (2019). Study on salt-tolerant physiological characteristics of cassava germplasm F200. Molecular Plant Breeding, 17, 2004-2010. |
| [28] | [吕瑞, 姚远, 段瑞军, 李瑞梅, 刘姣, 符少萍, 胡新文, 郭建春 (2019). 木薯种质“F200”耐盐生理特性探究. 分子植物育种, 17, 2004-2010.] |
| [29] | Magan N, Smith MK (1996). Isolation of the endophytes Lophodermium piceae and rhizosphaera kalkhoffii from Sitka spruce needles in poor and good growth sites and in vitro effects of environmental factors. Phyton-Annales Rei Botanicae, 36(3), 103-110. |
| [30] | Moghaddam MSH, Safaie N, Soltani J, Hagh-Doust N (2021). Desert-adapted fungal endophytes induce salinity and drought stress resistance in model crops. Plant Physiology & Biochemistry, 160, 225-238. |
| [31] | Mazumder S, Basu SK, Mukherjee M (2009). Laccase production in solid-state and submerged fermentation by Pleurotus ostreatus. Engineering in Life Sciences, 9, 45-52. |
| [32] | Pan XY, Qin Y, Yuan ZL (2018). Potential of a halophyte- associated endophytic fungus for sustaining Chinese white poplar growth under salinity. Symbiosis, 76, 109-116. |
| [33] | Pang YX, Wu Y, Qi L, Chen Y, Qin GH, Zhang CX, Wang H, Yang N, Cao BH (2019). Effects of salt stress on growth and physiological characteristics of ‘Luliu 1’ of Salix matsudana clones. Forest Science and Technology, (12), 17-22. |
| [33] | [庞元湘, 伍越, 祁琳, 陈颖, 秦光华, 张晨星, 王辉, 阳娜, 曹帮华 (2019). 盐胁迫对旱柳无性系‘鲁柳1号’幼苗生长和生理特性的影响. 林业科技通讯, (12), 17-22.] |
| [34] | Qi JY, Yin DC, Song RQ (2019). Effects of Suillus luteus on salt resistance of Pinus sylvestris var. mongolica seedlings. Journal of Shenyang Agricultural University, 50(1), 108-113. |
| [34] | [祁金玉, 尹大川, 宋瑞清 (2019). 褐环乳牛肝菌(Suillus luteus)对樟子松耐盐性的影响. 沈阳农业大学学报, 50(1), 108-113.] |
| [35] | Qi WC, Zhang L, Xu HB, Wang L, Jiao Z (2014). Physiological and molecular characterization of the enhanced salt tolerance induced by low-dose gamma irradiation in Arabidopsis seedlings. Biochemical and Biophysical Research Communications, 450, 1010-1015. |
| [36] | Shan TJ, Qin K, Xie YY, Zhang WH, Mao ZL, Wang J (2019). Secondary metabolites of endophytic fungi isolated from Casuarina equisetifolia and their bioactivities. Journal of South China Agricultural University, 40(3), 67-74. |
| [36] | [单体江, 秦楷, 谢银燕, 张伟豪, 毛子翎, 王军 (2019). 木麻黄内生真菌次生代谢产物及生物活性. 华南农业大学学报, 40(3), 67-74.] |
| [37] | Soccol CR, da Costa ESF, Letti LAJ, Karp SG, Woiciechowski AL, de Souza Vandenberghe LP (2017). Recent developments and innovations in solid state fermentation. Biotechnology Research and Innovation, 1, 52-71. |
| [38] | Strobel GA, Spang S, Kluck K, Hess WM, Sears J, Livinghouse T (2008). Synergism among volatile organic compounds resulting in increased antibiosis in Oidium sp. FEMS Microbiology Letters, 283, 140-145. |
| [39] | Sun CC, Zhao HY, Zheng CX (2017). Effects of NaCl stress on osmolyte and proline metabolism in Ginkgo biloba seedling. Plant Physiology Journal, 53, 470-476. |
| [39] | [孙聪聪, 赵海燕, 郑彩霞 (2017). NaCl胁迫对银杏幼树渗透调节物质及脯氨酸代谢的影响. 植物生理学报, 53, 470-476.] |
| [40] | Wang M, Chai BZ, Xi Z, Wan CY, Li NZ, Chen WC, Wan X, Huang FH (2021). Research progress of solid fermentation technology in biosynthesis of high value-added microbial metabolites by utilization of oil crop cake and meal. Chinese Journal of Oil Crop Sciences, 43, 322-337. |
| [40] | [王萌, 柴保中, 奚钊, 万楚筠, 李念祖, 陈文超, 万霞, 黄凤洪 (2021). 固体发酵技术在油料饼粕合成高附加值微生物代谢产物中的研究进展. 中国油料作物学报, 43, 322-337.] |
| [41] | Xie AQ, Hong W, Wu CZ (2012). Cold resistance nutrient characters with ten kinds of fungus in Eucalyptus urophylla × E. grandis. Scientia Silvae Sinicae, 48(6), 170-174. |
| [41] | [谢安强, 洪伟, 吴承祯 (2012). 桉树内生菌对尾巨桉幼苗抗寒生理指标的影响. 林业科学, 48(6), 170-174.] |
| [42] | Xie AQ, Hong W, Wu CZ, Feng L, Lin H, Li J, Fan HL (2011a). Effects of endophytic fungus in eucalyptus on the cold resistance of the seedling of E. urophylla × E. grandis. Journal of Fujian Agriculture and Forestry University (Natural Science Edition), 40(2), 138-144. |
| [42] | [谢安强, 洪伟, 吴承祯, 封磊, 林晗, 李键, 范海兰 (2011a). 桉树内生菌对尾巨桉幼苗抗寒性的影响. 福建农林大学学报(自然科学版), 40(2), 138-144.] |
| [43] | Xie AQ, Hong W, Wu CZ, Wen X, Hong T, Chen C (2011b). Effects of 10 strains of endogenesis fungi on photosynthesis in Eucalypt urophylla × E. grandis. Journal of Fujian College of Forestry, 31(1), 31-37. |
| [43] | [谢安强, 洪伟, 吴承祯, 文笑, 洪滔, 陈灿 (2011b). 10株桉树内生真菌对尾巨桉(E.urophylla×E.grandis)光合作用的影响. 福建林学院学报, 31(1), 31-37.] |
| [44] | Xu ZY, Xiao Z, He C, Lin Y, Li J, Ban YH (2019). Effects of dark endophytic fungi (DSE) on the growth and physiological characteristics of reed under three water conditions. Journal of Anhui Agricultural Sciences, 47(20), 48-53. |
| [44] | [徐舟影, 肖宗, 何聪, 林云, 李静, 班宜辉 (2019). 3种水分条件下深色有隔内生真菌(DSE)对芦苇生长及生理特性的影响. 安徽农业科学, 47(20), 48-53.] |
| [45] | Yang JX, Li QW, Guo ZY, Cai YN, Bi CZ (2019). Comprehensive evaluation on salt tolerance of three Prunus mume varieties. Journal of Northwest A&F University (Natural Science Edition), 47(8), 65-74. |
| [45] | [杨佳鑫, 李庆卫, 郭子燕, 蔡亚南, 毕春竹 (2019). 3个梅花品种幼苗耐盐性综合评价. 西北农林科技大学学报(自然科学版), 47(8), 65-74.] |
| [46] | Yao MZ, Chen LY, Cao S, Li XR, Wang LH, Wang J (2018). Effect of salt stress on physiological and biochemical characteristics and salt-tolerance of Vitex trifolia L. var. simplicifolia Cham. from different provenances. Journal of Northeast Forestry University, 46(10), 18-23. |
| [46] | [姚明志, 陈丽英, 曹森, 李晓荣, 王连红, 王静 (2018). 不同种源单叶蔓荆盐胁迫下生理生化特性及耐盐性评价. 东北林业大学学报, 46(10), 18-23.] |
| [47] | Ye BJ, Lan SR, Li MH, Lin WJ, Chen SP, Wu ML, Chen YB (2013). A floristic study of plants in campus of Fujian Agriculture and Forestry University. Journal of Fujian Agriculture and Forestry University (Natural Science Edition), 42(1), 51-56. |
| [47] | [叶宝鉴, 兰思仁, 李明河, 林文俊, 陈世品, 吴妙丽, 陈永滨 (2013). 福建农林大学校园植物区系特征. 福建农林大学学报(自然科学版), 42(1), 51-56.] |
| [48] | Ye GF, Lin DG, Xu JS, Lin WX, Lin JS, Lin J, Tan FL, Long XW (2000). Effects of soil salt stress on growth, physiological and biochemical characteristics of Casuarina equisetifolia. Protection Forest Science and Technology, (S1), 186-189. |
| [48] | [叶功富, 林德根, 徐俊森, 林武星, 林金顺, 林捷, 谭芳林, 隆学武 (2000). 土壤盐胁迫对木麻黄生长和生理生化特性的影响. 防护林科技, (S1), 186-189.] |
| [49] | Yuan ZL, Pan XY, Jin W (2019). Tree-associated symbiotic microbes and underlying mechanisms of ecological interactions: a case study of poplar. Acta Ecologica Sinica, 39, 381-397. |
| [49] | [袁志林, 潘雪玉, 靳微 (2019). 林木共生菌系统及其作用机制——以杨树为例. 生态学报, 39, 381-397.] |
| [50] | Zhang JJ, An SZ, Shi C, Liu H, Yang J (2017). Effects of endophytic fungi on seed germination and seedling physiological characteristics of Melica transsilvanica under salt stress. Chinese Journal of Grassland, 39(2), 59-64. |
| [50] | [张晶晶, 安沙舟, 施宠, 刘辉, 杨娇 (2017). 内生真菌侵染对盐胁迫下德兰臭草种子萌发及幼苗生理特性的影响. 中国草地学报, 39(2), 59-64.] |
| [51] | Zhang X, He KN, Shi CQ, Xu T, Wang H, Tang D (2017). Effects of salt stress on growth and physiological characteristics of Tamarix chinensis and Nitraria tangutorum seedlings. Journal of Northwest A&F University (Natural Science Edition), 45(1), 105-111. |
| [51] | [张雪, 贺康宁, 史常青, 徐特, 王辉, 唐达 (2017). 盐胁迫对柽柳和白刺幼苗生长与生理特性的影响. 西北农林科技大学学报(自然科学版), 45(1), 105-111.] |
| [52] | Zhang Y, Zhong CL, Han Q, Jiang QB, Chen Y, Chen Z, Pinyopusarerk K, Bush D (2016). Reproductive biology and breeding system in Casuarina equisetifolia (Casuarinaceae)—Implication for genetic improvement. Australian Journal of Botany, 64, 120-128. |
| [53] | Zhang Y, Zhong CL, Jiang QB, Chen Y, Chen Z (2008). Study on salt-tolerance ability in rooted cuttings of different Casuarina clones. Forest Research, (1), 91-95. |
| [53] | [张勇, 仲崇禄, 姜清彬, 陈羽, 陈珍 (2008). 木麻黄无性系水培苗抗盐性研究. 林业科学研究, (1), 91-95.] |
| [54] | Zhang YB, Deng AY, Zhuang TC, Lin P (2003). Relation between soil salinity in intertidal zone and electric conductivity. Ecology and Environmnet, (2), 164-165. |
| [54] | [张瑜斌, 邓爱英, 庄铁诚, 林鹏 (2003). 潮间带土壤盐度与电导率的关系. 生态环境, (2), 164-165.] |
| [55] | Zhang YQ, Huang R, Zuo LZ, Chen P, Li L (2020). Diversity of bacteria and allelopathic potential of their metabolites in differently aged Casuarina equisetifolia litter. Chinese Journal of Applied Ecology, 31, 2185-2194. |
| [55] | [张雅倩, 黄蕊, 左林芝, 陈盼, 李蕾 (2020). 海南岛不同林龄木麻黄凋落物内外细菌多样性及其化感潜力. 应用生态学报, 31, 2185-2194.] |
| [56] | Zhang ZL, Qu WJ (2004). Experimental Guidance of Plant Physiology. Higher Education Press, Beijing. 123-124. |
| [56] | 张志良, 瞿伟箐 (2004). 植物生理学实验指导. 高等教育出版社, 北京. 123-124.] |
| [57] | Zhu QQ (2019). Plant Endophytic Bacteria Salinicola tamaricis F01 Effects on Physiological and Biochemical Function of Suaeda salsa. Master degree dissertation, Shandong Normal University, Jinan. 72-78. |
| [57] | 朱巧巧 (2019). 植物内生菌Salinicola tamaricis F01对盐地碱蓬生理生化影响. 硕士学位论文, 山东师范大学, 济南. 72-78.] |
Options