荒漠区不同微生境下齿肋赤藓对一次降雪的生理生化响应

doi:10.3724/SP.J.1258.2014.00092

摘要/Abstract

摘要：

耐旱苔藓广泛分布于干旱半干旱荒漠地区, 对荒漠生态系统稳定性与功能多样性具有重要作用。齿肋赤藓(Syntrichia caninervis)是古尔班通古特沙漠苔藓结皮层的优势物种, 生于不同的微环境中。古尔班通古特沙漠冬、春季降雪频繁, 并能形成稳定的积雪层。目前关于降雪与微生境对齿肋赤藓生理生化特征影响的研究极为缺乏。该研究探讨了初冬一次降雪前后活灌丛、死灌丛和裸露地3种微生境下齿肋赤藓相关生理生化特征。结果表明, 与降雪前相比, 降雪后各微生境下齿肋赤藓植株的含水量、荧光活性、可溶性糖含量、超氧化物歧化酶(SOD)和过氧化物酶(POD)活性均有明显提高, 但脯氨酸、可溶性蛋白和丙二醛(MDA)含量有不同程度的降低。微生境对齿肋赤藓的生理指标有不同程度的影响, 而且与降雪具有显著的交互作用(脯氨酸除外)。降雪前后, 活灌丛下的齿肋赤藓具有较高的含水量和光合活性, 以及较低的保护酶(POD和SOD) 活性, 裸露地则表现出完全相反的特点。表明前者面临的胁迫最小, 生理活性最大, 但抗性较弱; 而后者具有更大的抗胁迫能力, 但生理活性低。降雪后, 脯氨酸、MDA、POD及SOD均与植株含水量呈显著负相关, 而荧光活性、可溶性糖及可溶性蛋白含量与植株含水量为显著正相关, 表明降雪降低了齿肋赤藓的水分胁迫程度, 改善并促进了生理活性与光合作用, 而且初冬的低温也起到了促进作用。

关键词: 古尔班通古特沙漠, 微生境, 生理生化特征, 降雪, 齿肋赤藓

Abstract:

Aims Water is the most constraining factor to the growth of plants in arid and semiarid regions of China. Biological soil crusts (BSCs) develop well in Gurbantünggüt Desert and Syntrichia caninervis is a dominant species in the moss crusts of this cold desert. Compared to other desert ecosystems, the Gurbantünggüt desert is home to stable and abundant snow cover in winter. The moisturizing and warming effects of snow cover provide the desert mosses with optimal growth conditions. Our objective in this study was to determine how S. caninervis shoots utilize the special snow resources under different microhabitats in early winter.
Methods The experiments were conducted from prior to the snowfall and until following the snow thawing at a long-term study site of the Gurbantünggüt Desert. We measured the physiological and biochemical characteristics in S. caninervis in three habitats: the live shrub, the dead shrub, an exposed area. The shoot water content, chlorophyll fluorescence, proline content, soluble sugar content, soluble protein content, malonyldialdehyde (MDA) content, peroxidase (POD) and superoxide dismutase (SOD) activity were compared.
Important findings The results showed that snowfall increased moss water content, the maximal photochemical efficiency of PSII (F_v/F_m), soluble sugar content, SOD and POD activity. The content of proline and MDA were reduced with snow melting. Microhabitats influenced the physiological characteristics in S. caninervis, with the effects varying with snowfall event. The water content and chlorophyll fluorescence activity were significantly higher in samples under the living shrub, while in the exposed area S. caninervis had lower water content and chlorophyll fluorescence activity regardless of the snowfall cover. These findings suggested that the S. caninervis plants under the loving shrub experienced the least stress and had the best physiological performance but weak resistance, and that those in exposed area were more stress tolerant and had poorer physiological performance. Following the snowfall, proline content, MDA content, POD and SOD activity all had significantly negative correlations with plant water content; whereas the soluble sugar and protein content displayed significantly positive correlations with plant water content. The results indicated that snowfall reduced the water stress in S. caninervis, and enhanced their physiological performance and photosynthesis, with the effects being facilitated by the low temperature of the early winter.

Key words: Gurbantünggüt Desert, microhabitats, physiological and biochemical characteristics, snowfall, Syntrichia caninervis

尹本丰,张元明. 荒漠区不同微生境下齿肋赤藓对一次降雪的生理生化响应. 植物生态学报, 2014, 38(9): 978-989. DOI: 10.3724/SP.J.1258.2014.00092

YIN Ben-Feng,ZHANG Yuan-Ming. Physiological and biochemical responses of Syntrichia caninervis at a snowfall event in different desert habitats. Chinese Journal of Plant Ecology, 2014, 38(9): 978-989. DOI: 10.3724/SP.J.1258.2014.00092

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.plant-ecology.com/CN/10.3724/SP.J.1258.2014.00092

https://www.plant-ecology.com/CN/Y2014/V38/I9/978

图/表 8

图1 实验期间不同微生境下土壤温度的变化。

Fig. 1 Variations in soil temperature in different microhabitats during the experiment.

表1 不同微生境下土壤理化性质的比较

Table 1 Comparison of soil physical and chemical properties among different microhabitats

变量 Variables	活灌丛 Live shrub	死灌丛 Dead shrub	裸露地 Exposed area
有机碳 Organic carbon (g·kg^-1)	3.721 ± 0.318^a	3.898 ± 0.737^a	2.300 ± 0.574^b
全氮 Total nitrogen (g·kg^-1)	0.475 ± 0.073^a	0.495 ± 0.048^a	0.301 ± 0.047^b
全磷 Total phosphorus (g·kg^-1)	0.400 ± 0.014^ab	0.445 ± 0.013^a	0.394 ± 0.059^b
全钾 Total potassium (g·kg^-1)	13.119 ± 0.249^a	12.977 ± 0.127^a	12.194 ± 0.136^b
总盐 Total salt (g·kg^-1)	0.576 ± 0.018^a	0.567 ± 0.079^a	0.514 ± 0.045^a
pH值 pH value	7.936 ± 0.031^a	7.672 ± 0.036^b	7.652 ± 0.262^b
电导率 Electrical conductivity (μS·cm^-1)	0.131 ± 0.009^a	0.129 ± 0.008^a	0.125 ± 0.016^a
雪前土壤含水量 Soil water content before snowfall (%)	2.844 ± 0.407^a	1.995 ± 0.608^b	1.731 ± 0.326^b
雪后土壤含水量 Soil water content after snow thaw (%)	4.236 ± 0.885^a	2.691 ± 0.779^b	2.605 ± 0.245^b

图2 初冬降雪前后不同微生境下齿肋赤藓含水量的比较。不同字母表示在降雪前或降雪后不同微生境下齿肋赤藓含水量差异显著(p < 0.05), *表示同一微生境降雪前后差异显著(p < 0.01)。

Fig. 2 Changes of water content in Syntrichia caninervis shoots during snowing event in different habitats. Different letters denote significant difference (p < 0.05) among microhabitats before or after snowfall, * denotes significant difference (p < 0.01) between shoot water contents before and after snowfall.

Fig. 3 Changes of maximum potential quantum efficiency of PSII (Fv/Fm) and actual photochemical efficiency (Y(II)) in Syntrichia caninervis shoots before and after snowfall event in different microhabitats. Different letters denote significant difference (p < 0.05) among microhabitats before or after snowfall, ** denotes significant difference (p < 0.01) between measurements before and after snowfall.

表2 降雪前后不同微生境下齿肋赤藓生化特征重复测量结果的方差分析

Table 2 Repeated measures ANOVA on the effects of microhabitats and snowfall on physiological and biochemical characteristics in Syntrichia caninervis

因子 Factor	脯氨酸含量 Proline content	可溶性糖含量 Soluble sugar content	可溶性蛋白含量 Soluble proteins content	丙二醛含量 MDA content	超氧化物歧化酶活性 SOD activity	过氧化物酶活性 POD activity
降雪 Snowfall	15.278^**	30.899^**	7.060^*	23.549^**	39.461^**	95.016^**
微生境 Microhabitats	5.875^*	32.455^**	4.643^*	1.240	2.009	12.811^**
降雪×微生境 Snowfall × microhabitats	2.050	83.368^**	9.784^**	5.668^*	12.807^**	31.718^**

图4 初冬降雪前后不同微生境下齿肋赤藓脯氨酸、可溶性糖和可溶性蛋白含量的比较。不同字母表示在降雪前或降雪后不同微生境下齿肋赤藓生理指标差异显著(p < 0.05), *和**表示同一微生境降雪前后差异显著(p < 0.05, p < 0.01), ns表示无差异(p > 0.05)。

Fig. 4 Effect of snowfall and microhabitats on proline, soluble sugar and soluble protein content in Syntrichia caninervis shoots. Different letters denote significant difference (p < 0.05) among microhabitats before or after snowfall; * and ** denote significant difference (p < 0.05 and p < 0.01) between measurements before and after snowfall; and ns denotes no significance.

图5 初冬降雪前后不同微生境下齿肋赤藓丙二醛(MDA)含量、超氧化物歧化酶(SOD)及过氧化物酶(POD)活性的比较。不同字母表示在降雪前或降雪后不同微生境下齿肋赤生理指标差异显著(p < 0.05), *和**表示同一微生境降雪前后差异显著(p < 0.05, p < 0.01), ns表示无差异(p > 0.05)。

Fig. 5 Effects of snowfall and microhabitats on malonyldialdehyde (MDA) content, superoxide dismutase (SOD) activity, peroxidase (POD) activity in Syntrichia caninervis shoots. Different letters denote significant difference (p < 0.05) among microhabitats before or after snowfall; * and ** denote significant difference (p < 0.05 and p < 0.01) between measurements before and after snowfall; and ns denotes no significance.

表3 降雪前后不同微生境下齿肋赤藓生化特征与环境因子间的相关系数

Table 3 Correlation coefficients among physiological traits in Syntrichia caninervis shoots and environmental factors in different microhabitats before and after snowfall

变量 Variables	F_v/F_m	Pro	SSu	SPr	MDA	POD	SOD	T
降雪前 Before snowfall
Wc	0.347	-0.802^**	-0.788^*	-0.336	-0.045	0.403	0.390	-0.590^*
F_v/F_m		-0.816^**	-0.782^**	-0.091	-0.433	-0.178	-0.472	-0.925^**
Pro			0.747^*	-0.033	0.593^*	0.042	0.289	0.623^*
SSu				0.023	0.577	0.181	0.341	0.190
SPr					-0.493	-0.945^**	-0.852^**	0.022
MDA						0.471	0.673^*	0.362
POD							0.405	0.022
SOD								0.332
降雪后 After snowfall
Wc	0.907^**	-0.725^**	0.809^**	0.960^**	-0.580^*	-0.829^**	-0.619^*	-0.952^**
F_v/F_m		-0.667^**	-0.786^**	0.857^**	0.291	-0.952^**	-0.713^**	-0.903^**
Pro			-0.446	-0.763^**	0.246	0.583^*	0.578^*	0.513
SSu				0.801^**	0.404	-0.681^*	-0.250	-0.947^**
SPr					0.117	-0.885^**	-0.701^**	-0.892^**
MDA						-0.342	0.200	-0.454
POD							0.771^**	0.849^**
SOD								0.442

参考文献 59

[1]	Belnap J, Harper KT, Warren SD (1994). Surface disturbance of cryptobiotic soil crusts: nitrogenase activity, chlorophyll content, and chlorophyll degradation. Arid Land Research and Management, 8, 1-8.
[2]	Benassi M, Stark LR, Brinda JC, Mcletchie DN, Bonine M, Mishler BD (2011). Plant size, sex expression and sexual reproduction along an elevation gradient in a desert moss. The Bryologist, 114, 277-288.
[3]	Brotherson JD, Rushforth SR (1983). Influence of cryptogamic crusts on moisture relationships of soils in Navajo National Monument, Arizona. Western North American Naturalist, 43, 73-78.
[4]	Cao T, Li QY (2009). Research advances in molecular ecology of bryophytes. Journal of Shanghai Normal University (Natural Sciences), 38, 651-657. (in Chinese with English abstract)
	[ 曹同, 李倩影 (2009). 苔藓植物分子生态学研究进展. 上海师范大学学报(自然科学版), 38, 651-657.]
[5]	Chen WJ, Zhang N, Hang LL, Wang Y, Ji MC (2013). Influence of shading during the processes of drought stress and re-watering on the physiological and biochemical characteristics of Haplocladium microphyllum. Chinese Journal of Applied Ecology, 24, 57-62. (in Chinese with English abstract)
	[ 陈文佳, 张楠, 杭璐璐, 王媛, 季梦成 (2013). 干旱胁迫与复水过程中遮光对细叶小羽藓的生理生化影响. 应用生态学报, 24, 57-62.]
[6]	Cole C, Stark LR, Bonine ML, Mcletchie DN (2010). Transplant survivorship of bryophyte soil crusts in the Mojave Desert. Restoration Ecology, 18, 198-205. DOI URL
[7]	Cornelissen JH, Lang SI, Soudzilovskaia NA, During HJ (2007). Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Annals of Botany, 99, 987-1001. URL PMID
[8]	Crowe JH, Carpenter JF, Crowe LM (1998). The role of vitrification in anhydrobiosis. Annual Review of Physiology, 60, 73-103. URL PMID
[9]	Fan LL, Ma J, Wu LF, Xu GQ, Li Y, Tang LS (2012). Response of the herbaceous layer to snow variability at the south margin of the Gurbantunggut Desert of China. Chinese Journal of Plant Ecology, 36, 126-135. (in Chinese with English abstract) DOI URL
	[ 范连连, 马健, 吴林峰, 徐贵青, 李彦, 唐立松 (2012). 古尔班通古特沙漠南缘草本层对积雪变化的响应. 植物生态学报, 36, 126-135.] DOI URL
[10]	Gao LQ, Zhao YG, Qin NQ, Zhang GX (2013). Effects of biological soil crust on soil erodibility in hilly Loess Plateau region of Northwest China. Chinese Journal of Applied Ecology, 24, 105-112. (in Chinese with English abstract) URL PMID
	[ 高丽倩, 赵允格, 秦宁强, 张国秀 (2013). 黄土丘陵区生物结皮对土壤可蚀性的影响. 应用生态学报, 24, 105-112.] URL PMID
[11]	Hamerlynck EP, Csintalan Z, Nagy Z, Tuba Z, Goodin D, Henebry GM (2002). Ecophysiological consequences of contrasting microenvironments on the desiccation tolerant moss Tortula ruralis. Oecologia, 131, 498-505. DOI URL PMID
[12]	Herrnstadt I, Kidron GJ (2005). Reproductive strategies of Bryum dunense in three microhabitats in the Negev Desert. The Bryologist, 108, 101-109.
[13]	Khandelwal A, Cho S, Marella H, Sakata Y, Perroud PF, Quatrano RS (2010). Role of ABA and ABI3 in desiccation tolerance. Science, 327, 546-546. DOI URL
[14]	Kidron GJ, Vonshak A, Abeliovich A (2009). Microbiotic crusts as biomarkers for surface stability and wetness duration in the Negev Desert. Earth Surface Processes and Landforms, 34, 1594-1604.
[15]	Li XR, Zhang JG, Wang XP, Liu LC, Xiao HL (2000). Study on soil microbiotic crust and its influences on sand-fixing vegetation in arid desert region. Acta Botanica Sinica, 42, 965-970. (in English with Chinese abstract)
	[ 李新荣, 张景光, 王新平, 刘立超, 肖洪浪 (2000). 干旱沙漠区土壤微生物结皮及其对固沙植被影响的研究. 植物学报, 42, 965-970.]
[16]	Li XR, Zhang YM, Zhao YG (2009). A study of biological soil crusts: recent development, trend and prospect. Advances in Earth Science, 24, 11-24. (in Chinese with English abstract)
	[ 李新荣, 张元明, 赵允格 (2009). 生物土壤结皮研究: 进展、前沿与展望. 地球科学进展, 24, 11-24.]
[17]	Maria Sgherri CL, Loggini B, Puliga S, Navari-izzo F (1994). Antioxidant system in Sporobolus stapfianus: changes in response to desiccation and rehydration. Phytochemistry, 35, 561-565.
[18]	Martin CE, Churchill SP (1982). Chlorophyll concentrations and a/b ratios in mosses collected from exposed and shaded habitats in Kansas. Journal of Bryology, 12, 297-304.
[19]	Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003). Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environmental and Experimental Botany, 49, 69-76.
[20]	Nasrulhaq-Boyce A, Mohamed H, Lim A, Barakbah SS, Yong KT, Nor DM (2011). Comparative morphological and photosynthetic studies on three Malaysian species of Pogonatum from habitats of varying light irradiances. Journal of Bryology, 33, 35-41.
[21]	Oliver MJ, Velten J, Mishler BD (2005). Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integrative and Comparative Biology, 45, 788-799. DOI URL PMID
[22]	Oliver MJ, Wood AJ, O’Mahony P (1997). How some plants recover from vegetative desiccation: a repair based strategy. Acta Physiologiae Plantarum, 19, 419-425.
[23]	Pintado A, Sancho LG, Green T, Blanquer JM, Lázaro R (2005). Functional ecology of the biological soil crust in semiarid SE Spain: sun and shade populations of Diploschistes diacapsis(Ach.) Lumbsch. The Lichenolo- gist, 37, 425-432.
[24]	Proctor MC (2000). The bryophyte paradox: tolerance of desiccation, evasion of drought. Plant Ecology, 151, 41-49.
[25]	Proctor MC, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD (2007). Desiccation-tolerance in bryophytes: a review. The Bryologist, 110, 595-621.
[26]	Proctor MC, Smirnoff N (2000). Rapid recovery of photosystems on rewetting desiccation-tolerant mosses: chlorophyll fluorescence and inhibitor experiments. Journal of Experimental Botany, 51, 1695-1704. DOI URL PMID
[27]	Qin NQ, Zhao YG (2011). Responses of biological soil crust to and its relief effect on raindrop kinetic energy. Chinese Journal of Applied Ecology, 22, 2259-2264. (in Chinese with English abstract) URL PMID
	[ 秦宁强, 赵允格 (2011). 生物土壤结皮对雨滴动能的响应及削减作用. 应用生态学报, 22, 2259-2264.] URL PMID
[28]	Schlensog M, Schroeter B, Pannewitz S, Green TGA (2003). Adaptation of Mosses and Lichens to Irradiance Stress in Maritime and Continental Antarctic Habitats. Antarctic Biology in a Global Context Backhuys Publisher, Leiden.
[29]	Shao YJ, Shan L, Li GM (2006). Comparison of osmotic regulation and antioxidation between sorghum and maize seedlings under soil drought stress and (water) recovering conditions. Chinese Journal of Eco-Agriculture, 14, 68-70. (in Chinese with English abstract)
	[ 邵艳军, 山仑, 李广敏 (2006). 干旱胁迫与复水条件下高粱、玉米苗期渗透调节及抗氧化比较研究. 中国生态农业学报, 14, 68-70.]
[30]	Shen L, Guo SL, Wu Y, Cao T, Glime JM (2011). Physiolo- gical responses of Hypnum fertile Sendtn.(Musci: Hypnaceae) to short-term extreme temperature stress. Bulletin of Botanical Research, 31, 40-48. (in English with Chinese abstract)
	[ 沈蕾, 郭水良, 杨武, 曹同, Glime JM (2011). 多蒴灰藓(苔藓植物门: 藓纲)对短期极端温度的生理响应. 植物研究, 31, 40-48.]
[31]	Stark LR, McLetchie DN, Eppley SM (2010). Sex ratios and the shy male hypothesis in the moss Bryum argenteum(Bryaceae). The Bryologist, 113, 788-797.
[32]	Stark LR, Nichols L, McLetchie DN, Bonine ML (2005). Do the sexes of the desert moss Syntrichia caninervis differ in desiccation tolerance? A leaf regeneration assay. International Journal of Plant Sciences, 166, 21-29.
[33]	Stark LR, Nichols L, McLetchie DN, Smith SD, Zundel C (2004). Age and sex-specific rates of leaf regeneration in the Mojave Desert moss Syntrichia caninervis. American Journal of Botany, 91, 1-9. DOI URL PMID
[34]	Su YG, Wu L, Zhou ZB, Liu YB, Zhang YM (2013). Carbon flux in deserts depends on soil cover type: a case study in the Gurbantunggute Desert, North China. Soil Biology & Biochemistry, 58, 332-340.
[35]	Sun SQ, Wang GX, Luo J, Song HT, Yang G (2009). Response and adaption of bryophytes to the changes of environmental factors. Acta Botanica Boreali-Occidentalia Sinica, 29, 2360-2365. (in Chinese with English abstract)
	[ 孙守琴, 王根绪, 罗辑, 宋洪涛, 杨刚 (2009). 苔藓植物对环境变化的响应和适应性. 西北植物学报, 29, 2360-2365.]
[36]	Tao Y, Zhang YM (2012). Effects of leaf hair points on dew deposition and rainfall evaporation rates in moss crusts dominated by Syntrichia caninervis, Gurbantunggut Desert, Northwestern China. Acta Ecologica Sinica, 32, 7-16. (in Chinese with English abstract)
	[ 陶冶, 张元明 (2012). 叶片毛尖对齿肋赤藓结皮凝结水形成及蒸发的影响. 生态学报, 32, 7-16.]
[37]	Tian GQ, Bai XL, Xu J, Wang XD (2005). Experimental studies on natural regeneration and artificial cultures of moss crusts on fixed dunes in the Tengger Desert. Acta Phytoecologica Sinica, 29, 164-169. (in Chinese with English abstract)
	[ 田桂泉, 白学良, 徐杰, 王先道 (2005). 腾格里沙漠固定沙丘藓类植物结皮层的自然恢复及人工培养试验研究. 植物生态学报, 29, 164-169.]
[38]	Wang HL, Zhang YM (2008). Study on the morphological and anatomical structures of desert mosses in biotic crust in the Gurbantunggut Desert. Arid Zone Research, 25, 363-370. (in Chinese with English abstract)
	[ 王红玲, 张元明 (2008). 古尔班通古特沙漠生物结皮中藓类植物形态解剖特征. 干旱区研究, 25, 363-370.]
[39]	Wang XQ, Zhang YM, Zhang WM, Han ZW (2004). Wind tunned experiment of biological soil crust effect on wind erodibility of sand surface in Gurbantunggut Desert, Xin- jiang. Journal of Glaciology and Geocryology, 26, 632-638. (in Chinese with English abstract)
	[ 王雪芹, 张元明, 张伟民, 韩致文 (2004). 古尔班通古特沙漠生物结皮对地表风蚀作用影响的风洞实验. 冰川冻土, 26, 632-638.]
[40]	Wu N, Wei ML, Zhang YM (2009). Membrane permeability of Syntrichia caninervis in response to dehydration and rehydration in biological soil crust. Progress in Nature Science, 19, 942-951. (in Chinese)
	[ 吴楠, 魏美丽, 张元明 (2009). 生物土壤结皮中刺叶赤藓质膜透性对脱水, 复水过程的响应. 自然科学进展, 19, 942-951.]
[41]	Wu N, Zhang YM, Downing A, Aanderud ZT, Tao Y, Williams S (2014). Rapid adjustment of leaf angle explains how the desert moss, Syntrichia caninervis, copes with multiple resource limitations during rehydration. Functional Plant Biology, 41, 168-177. DOI URL PMID
[42]	Xu J, Bai XL, Tian GQ, Yao YP, Gao TY (2005). Study on moss: the content of amino acid, the feature of nutritive elements and its resistance to draught in the biotic crusts in arid and semi-arid regions. Acta Ecologica Sinica, 25, 1247-1255. (in Chinese with English abstract)
	[ 徐杰, 白学良, 田桂泉, 姚一萍, 高天云 (2005). 干旱半干旱地区生物结皮层藓类植物氨基酸和营养物质组成特征及适应性分析. 生态学报, 25, 1247-1255.]
[43]	Xu J, Bai XL, Yang C, Zhang P (2003). Study on diversity and binding-sand effect of moss on biotic crusts of fixed dunes. Acta Phytoecologica Sinica, 27, 545-551. (in Chinese with English abstract)
	[ 徐杰, 白学良, 杨持, 张萍 (2003). 固定沙丘结皮层藓类植物多样性及固沙作用研究. 植物生态学报, 27, 545-551.]
[44]	Xuan XM (2004). Research on Environment Physiology Character of the Drought-Enduring Bryophyte. Master degree dissertation, Shanghai Jiaotong University, Shanghai. (in Chinese with English abstract)
	[ 玄雪梅 (2004). 耐旱苔藓植物环境生理学特性的研究. 硕士学位论文, 上海交通大学, 上海.]
[45]	Zhang J, Zhang YM (2011). Effects of freezing and thawing on chlorophyll fluorescence of Syntrichia caninervis in biological soil crusts. Journal of Desert Research, 31, 1479-1487. (in Chinese with English abstract)
	[ 张静, 张元明 (2011). 冻融过程对生物结皮中齿肋赤藓叶绿素荧光特性的影响. 中国沙漠, 31, 1479-1487.]
[46]	Zhang J, Zhang YM (2014). Influence of simulated rainfall on the physiological characteristics of Syntrichia caninervis. Journal of Desert Research, 34, 433-440. (in Chinese with English abstract) DOI URL
	[ 张静, 张元明 (2014). 模拟降雨对齿肋赤藓(Syntrichia caninervis)生理特性的影响. 中国沙漠, 34, 433-440.] DOI URL
[47]	Zhang J, Zhang YM, Downing A, Cheng JH, Zhou XB, Zhang BC (2009). The influence of biological soil crusts on dew deposition in Gurbantunggut Desert, Northwestern China. Journal of Hydrology, 379, 220-228.
[48]	Zhang JX, Kirkham MB (1994). Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant & Cell Physiology, 35, 785-791.
[49]	Zhang YF, Wang XP, Hu R, Pan YX (2013). Effects of shrubs and precipitation on spatial-temporal variation of soil temperature at the microhabitats induced by desert shrubs. Journal of Desert Research, 33, 536-542. (in Chinese with English abstract)
	[ 张亚峰, 王新平, 虎瑞, 潘颜霞 (2013). 荒漠灌丛微生境土壤温度的时空变异特征——灌丛与降水的影响. 中国沙漠, 33, 536-542.]
[50]	Zhang YM (2005). Microstructure and development characters in early stage of biological soil crust of desert. Chinese Science Bulletin, 50, 42-47. (in Chinese)
	[ 张元明 (2005). 荒漠地表生物土壤结皮的微结构及其早期发育特征. 科学通报, 50, 42-47.]
[51]	Zhang YM, Chen J, Wang L, Wang XQ, Gu ZH (2007). The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China. Journal of Arid Environments, 68, 599-610.
[52]	Zhang YM, Pan HX, Pan BR (2004). Distribution characteristics of biological crust on sand dune surface in Gurbantunggut Desert, Xinjiang. Journal of Soil and Water Conservation, 18, 61-64. (in Chinese with English abstract)
	[ 张元明, 潘惠霞, 潘伯荣 (2004). 古尔班通古特沙漠不同地貌部位生物结皮的选择性分布. 水土保持学报, 18, 61-64.]
[53]	Zhang YS, Huang X, Chen YF (2009). Experiment Course of Plant Physiology. Higher Education Press, Beijing. (in Chinese)
	[ 张以顺, 黄霞, 陈云凤 (2009). 植物生理学实验教材. 高等教育出版社, 北京.]
[54]	Zhang ZM, Dai LX, Song WW, Ding H, Ci DW, Kang T, Ning TY, Wan SB (2013). Effect of drought stresses at different growth stages on peanut leaf protective enzyme activities and osmoregulation substances content. Acta Agronomica Sinica, 39, 133-141. (in Chinese with English abstract)
	[ 张智猛, 戴良香, 宋文武, 丁红, 慈敦伟, 康涛, 宁堂原, 万书波 (2013). 干旱处理对花生品种叶片保护酶活性和渗透物质含量的影响. 作物学报, 39, 133-141.]
[55]	Zheng XJ, Li S, Wu LF, Li Y, Qin HB (2012). Eco- hydrological effect of shrub rime in the Gurbantunggut Desert. Journal of Glaciology and Geocryology, 34, 942-949. (in Chinese with English abstract)
	[ 郑新军, 李嵩, 吴林峰, 李彦, 秦海波 (2012). 古尔班通古特沙漠灌丛雾凇的生态水文学效应. 冰川冻土, 34, 942-949.]
[56]	Zheng YP, Zhao JC, Zhang BC, Zhang YM (2009). Morpholo- gical and structural adaptation and characteristics of protonemal development of Syntrichia caninervis in the mosses crust layer. Journal of Desert Research, 29, 878-884. (in Chinese with English abstract)
	[ 郑云普, 赵建成, 张丙昌, 张元明 (2009). 荒漠藓类结皮层中齿肋赤藓形态结构适应性及其原丝体发育特征. 中国沙漠, 29, 878-884.]
[57]	Zhou HF, Li Y, Tang Y, Zhou BJ, Xu HW (2009). The characteristics of the snow-cover and snowmelt water storage in Gurbantunggut Desert. Arid Zone Research, 26, 312-317. (in Chinese with English abstract) DOI URL
	[ 周宏飞, 李彦, 汤英, 周宝佳, 徐宏伟 (2009). 古尔班通古特沙漠的积雪及雪融水储存特征. 干旱区研究, 26, 312-317.] DOI URL
[58]	Zhou HF, Zhou BJ, Dai Q (2010). Observational analysis of rime condensation on plants over the Gurbantunggut Desert in China. Advances in Water Science, 21, 56-62. (in Chinese with English abstract)
	[ 周宏飞, 周宝佳, 代琼 (2010). 古尔班通古特沙漠植物雾凇凝结特征. 水科学进展, 21, 56-62.]
[59]	Zhu Z, Jiang JY, Jiang CJ, Li W (2011). Effects of low temperature stress on SOD activity, soluble protein content and soluble sugar content in Camellia sinensis leaves. Journal of Anhui Agricultural University, 38, 24-26. (in Chinese with English abstract)
	[ 朱政, 蒋家月, 江昌俊, 李雯 (2011). 低温胁迫对茶树叶片SOD、可溶性蛋白和可溶性糖含量的影响. 安徽农业大学学报, 38, 24-26.]