全 文 ：植物生态学报 2013, 37 (5): 454–463 doi: 10.3724/SP.J.1258.2013.00047
Chinese Journal of Plant Ecology http://www.plant-ecology.com
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收稿日期Received: 2012-12-27 接受日期Accepted: 2013-03-12
* 通讯作者Author for correspondence (E-mail: gaoyan1960@sohu.com)
迷迭香对干旱胁迫的生理响应及其诱导挥发性有
机化合物的释放
刘 芳1 左照江1 许改平1 吴兴波1 郑 洁1 高荣孚2 张汝民1 高 岩1*
1浙江农林大学亚热带森林培育国家重点实验室培育基地, 浙江临安 311300; 2北京林业大学生物科学与技术学院, 北京 100083
摘 要 为探讨干旱胁迫对迷迭香(Rosmarinus officinalis)生理生化特性及挥发性有机化合物(VOC)释放规律的影响, 该文采
用盆栽称重控水法研究了轻度(LD)、中度(MD)和重度(SD)干旱胁迫对迷迭香二年生实生苗叶片细胞膜透性、可溶性糖、可
溶性蛋白质和丙二醛(MDA)含量以及脂氧合酶和抗氧化保护酶活性的影响, 并采用热脱附/气相色谱/质谱联用技术对不同干
旱胁迫下迷迭香释放的挥发性有机化合物成分进行了分析。结果表明: 干旱胁迫对迷迭香叶片可溶性糖和可溶性蛋白质含量
有明显的影响, MD和SD处理12天时其含量极显著地增加(p < 0.01), 与对照相比可溶性糖分别增加了51.5%和87.4%, 可溶性
蛋白质含量分别增加了0.82和1.40倍。在MD和SD胁迫下, 超氧化物歧化酶、过氧化物酶和过氧化氢酶对干旱胁迫的响应存
在一定差异, 表现为相互协调的作用。随着干旱胁迫时间的延长, 迷迭香体内MDA含量极显著地增加(p < 0.01), 细胞膜损伤
率显著增加。分析显示, 迷迭香释放的VOC主要是萜烯类化合物, 占总量的46.0%以上; 随着干旱胁迫增强, 迷迭香释放的
VOCs总量减少, 种类增多; LD、MD和SD胁迫处理萜烯类化合物相对含量与对照相比分别增加了14.4%、17.0%和23.7%; 干
旱胁迫还明显诱导绿叶挥发物(green leaf volatiles)和醛类化合物的释放, 诱导产生了2-己烯醛、叶醇、山梨醛和癸醛4种新组
分。研究表明: 干旱胁迫条件下, 迷迭香能够通过调节保护酶活性、渗透调节物质含量和释放VOCs来提高抗旱性。
关键词 干旱胁迫, 脂氧合酶, 渗透调节物质, 保护酶, 迷迭香, 挥发性有机化合物
Physiological responses to drought stress and the emission of induced volatile organic com-
pounds in Rosmarinus officinalis
LIU Fang1, ZUO Zhao-Jiang1, XU Gai-Ping1, WU Xing-Bo1, ZHENG Jie1, GAO Rong-Fu2, ZHANG Ru-Min1, and
GAO Yan1*
1The Nurturing Station for the State Key Laboratory of Subtropical Silviculture, Zhejiang Agriculture and Forestry University, Lin’an, Zhejiang 311300, China;
and 2College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China
Abstract
Aims Drought is one of the numerous environmental factors which affect the growth and development of plants,
and it becomes more severe in many regions of the world due to climate change. To examine the mechanisms of
responses of the plant Rosemarinus offcinalis to drought stress, we measured the physiological and biochemical
changes and volatile organic compounds (VOCs) emission of 2-year-old seedlings of this species under conditions
of light drought (LD), intermediate drought (MD) and severe drought (SD).
Methods The VOCs emission was measured using the dynamic headspace air-circulation method, and the com-
position and content of VOCs were analyzed using the thermal desorption system/gas chromatography/mass spec-
trometer technique (TDS-GC-MS). We measured ion leakage of cell membranes and the content of soluble sugar,
soluble protein and malondialdehyde (MDA), activities of lipoxygenase and protective enzymes of R. offcinalis
under the different drought treatments.
Important findings The content of osmotic adjustment materials in R. offcinalis leaves was significantly influ-
enced by drought stress. The content of soluble sugar was increased by 51.5% and 87.4% (p < 0.01) under MD
and SD stresses after 12 days, respectively. The content of soluble protein was increased by 82% and 140% (p <
0.01), respectively. There were differences among the activity of superoxide dismutase (SOD), peroxidase (POD)
and catalase (CAT) in response to drought stress, which was a coordination reaction of those three enzymes to the
stress. With prolonged drought stress, the MDA content (p < 0.01) and cell injury rate (p < 0.05) were increased
significantly. Terpenoids were the main components of R. offcinalis VOCs and their relative content was more
刘芳等: 迷迭香对干旱胁迫的生理响应及其诱导挥发性有机化合物的释放 455

doi: 10.3724/SP.J.1258.2013.00047
than 46% of the total VOCs. Compared with the control, it was increased by 14.4%, 17.0% and 23.7%, respec-
tively, under LD, MD and SD stresses, respectively. Meanwhile, green leaf volatiles (GLVs) and aldehydes were
markedly induced by drought stress, and (E)-2-hexenal, leaf alcohol, sorbaldehyde and n-decanal were newly
found under the drought stress. The results indicated that R. offcinalis could enhance its drought-resistant ability
by adjusting activities of protective enzymes, improving contents of osmotic adjustment materials and releasing
VOCs.
Key words drought stress, lipoxygenase, osmotic adjustment material, protective enzyme, Rosmarinus offici-
nalis, volatile organic compounds

随着全球气候的变化, 干旱对植物生长和作物
产量的影响越来越突出, 成为制约世界各地农林业
可持续发展的关键环境因子(Thakur et al., 2010;
Cramer et al., 2011)。目前众多学者从植物形态结构
(Jaleel et al., 2009; Potters et al., 2009; 金雅琴等,
2012)、生长发育(Bengough et al., 2011)、代谢特性
(Gill & Tuteja, 2010; 文瑛等 , 2012)和分子机制
(Miller et al., 2010; 张小丰等, 2011; Atkinson &
Urwin, 2012)等方面对植物抗逆性机理开展了大量
的研究工作。
植物体内次生代谢释放的挥发性有机化合物
(volatile organic compounds, VOCs)有几万种, 其中
已经鉴别出的有1 700多种(Dicke & Loreto, 2010),
它们在调节植物生长(左照江等, 2010)、发育和繁衍
(Dudareva et al., 2004; Laothawornkitkul et al.,
2008)、抵抗植食性昆虫和病原菌侵害(Baldwin et
al., 2006; Holopainen & Gershenzon, 2010)等方面都
具有重要的信号作用。近几年研究发现, 植物释放
VOCs在增强抵抗非生物胁迫能力方面也发挥着重
要的作用(Holopainen & Gershenzon, 2010; Loreto &
Schnitzler, 2010; 周帅等, 2012)。对垂枝桦(Betula
pendula)和欧洲山杨(Populus tremula)的研究发现,
高温胁迫会诱导萜烯类和绿叶性气体释放量增加
(Ibrahim et al., 2010); 光照不足或者过强都会减少
植物VOCs的释放量(Gouinguené & Turlings, 2002)。
干旱胁迫对植物VOCs释放的影响与胁迫程度密切
相关, 适度干旱胁迫导致Quercus suber单萜类化合
物释放量增加(Staudt et al., 2008; Lavoir et al.,
2009); Filella等(2009)对Pinus halepensis的研究发
现, 适度的干旱胁迫导致短链含氧VOCs释放量增
加; 而Grote等(2010)经过多年研究发现, 重度干旱
胁迫导致Quercus ilex单萜释放量比对照降低了
67%。
迷迭香(Rosmarinus officinalis)又名情人草, 唇
形科迷迭香属多年生常绿亚灌木, 原产于地中海沿
岸一带, 战国时期从西域引入我国种植, 当时仅用
于闻其特有香味。迷迭香株形优美, 香味浓烈, 抗旱
性极强, 是一种被广泛应用的园林芳香植物。近几
年, 对迷迭香的研究主要集中在精油组分分析(黄
宏妙等, 2012)、提取工艺(王珲等, 2011; Sui et al.,
2012), 以及精油的抗氧化物功能(Tai, 2012; 袁干军
等, 2012)等方面。迷迭香在自然状态下释放的VOCs
是否与其抗旱性有关鲜见报道。因此, 本研究采用
控水法模拟干旱胁迫, 利用动态顶空气体循环法和
热脱附/气相色谱/质谱联用技术(TDC-GC-MS)测定
了迷迭香释放VOCs成分的变化; 同时, 测定了迷
迭香叶片渗透调节物质含量以及脂氧酶和保护酶活
性的变化, 以期从迷迭香释放VOCs和生理生化角
度揭示其对干旱胁迫的适应机制, 为进一步研究植
物释放VOCs对非生物胁迫响应机理提供理论依
据。
1 材料和方法
1.1 供试材料及处理
供试材料为迷迭香2年生实生苗(江苏省宿迁谊
园花卉盆景苗木公司提供), 苗高约20 cm。2012年4
月栽置于盛有培养土(泥炭:沙土:蛭石=1:2:1, 干质
量1.8 kg)的花盆中(直径18 cm, 高20 cm), 每盆1株。
盆栽苗置于温室中, 在充足的水分条件下培养恢复
1个月后实施控水处理。选取质量相近的盆栽苗((40
± 5) g) 24盆, 随机分为4组, 分别进行干旱胁迫处
理。设正常浇水(CK, 75%田间持水量(FC))、轻度干
旱(LD, 60% FC)、中度干旱(MD, 40% FC)和重度干
旱(SD, 20% FC) 4种处理, 每种处理6盆。采用称重
法控制土壤水分含量, 每天傍晚称重并补充各处理
消耗的水分。每4天测定1次各项指标, 重复3次。
1.2 实验方法
酶液提取: 称取迷迭香枝条中上部成熟叶片
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0.5 g, 加入适量预冷的0.05 mol·L–1的pH 7.8磷酸缓
冲溶液, 充分冰浴研磨后, 定容至25 mL。4 ℃下
10 000 r·min–1离心20 min, 回收上清液用于酶活性
及可溶性蛋白、可溶性糖和MDA含量的测定。
脂氧合酶 (LOX)活性的测定参照Hatanaka
(1993)的方法并进行改进。底物配制: 在2 mL 0.2
mol·L–1的硼酸缓冲液 (pH 9.0)中加入 0.1 mL
Tween-20混匀, 滴加0.1 mL亚油酸后充分混匀, 再
加入1 mol·L–1 NaOH溶液0.2 mL, 并保证此时的溶
液澄清, 然后加入上述硼酸缓冲液18 mL, 再加水
定容至50 mL, –20 ℃保存备用。3 mL反应体系中含
有0.1 mL底物、2.8 mL磷酸缓冲液(0.1 mol·L–1, pH
7.0) 和0.1 mL酶液, 测定反应体系3 min内在234
nm波长处吸光度的变化。酶活性定义: 234 nm波长
处, 以亚油酸为底物, 3 mL反应体系吸光度每min增
加0.1为一个酶活性单位U。
超 氧 化 物 歧 化 酶 (SOD) 活 性 测 定 参 照
Giannopolitis和Riess (1977)的方法, 以抑制NBT光
氧化还原50%的酶量为一个酶活性单位U。过氧化
物酶 (POD)和过氧化氢酶 (CAT)活性测定参照
Chance和Maehly (1955)的方法, POD以时间扫描方
式测定4 min内吸光值的变化, 取线性部分, 计算每
min吸光度变化值; CAT以1 min内吸光度减少0.01
的酶量为1个酶活单位U。可溶性蛋白含量测定参照
Bradford (1976)的方法; 可溶性糖含量测定采用蒽
酮比色法。
丙二醛(MDA)含量测定参照Zhang和Kirkham
(1994)的方法。取上述酶提取液1 mL, 加入三氯乙
酸和TBA混合液4 mL, 沸水中加热15 min, 冰浴速
冷, 离心, 取上清液于分光光度计上分别测定450、
532和600 nm处的吸光值, 计算MDA含量。
细胞膜伤害率采用电导仪法测定, 取迷迭香枝
条中上部成熟叶片0.2 g, 放入去离子水中洗净, 每
片叶片均匀剪为3段, 放入盛有20 mL去离子水的小
烧杯中, 室温下放置30 min (每5 min搅拌一次)后测
定电导率, 然后加热小烧杯煮10 min后再次测定电
导率, 伤害率计算公式:
伤害率(%) =
100)
1
11( ×−
−− 对照煮后电导值对照煮前电导值
处理煮后电导值处理煮前电导值
1.3 VOCs采集及分析方法
干旱胁迫处理24天后, 在9:00–11:00, 采用动
态顶空气体循环采集法收集整株迷迭香VOCs, 气
体流量0.1 m3·min–1, 采样时间20 min。VOCs成分分
析采用TDS-GC-MS法。仪器及参数设置条件参照
Gao等(2005)的方法。TDS (TD3型, Gerstel GmbH &
Co.KG, mülheim, Germany)工作条件: 载气压力20
kPa; 进样口温度250 ℃; 热脱附温度250 ℃, 10
min; 冷阱温度–100 ℃, 3 min; 进样时冷阱骤然升
至 260 ℃。GC (7890A型 , Agilent Technologies
Company, Santa Clara, USA)工作条件: 色谱柱为30
m × 250 μm × 0.25 μm的HP-5MS柱; 升温程序: 初
始温度40 ℃, 保持4 min后, 以6 ℃·min–1速率升至
250 ℃, 保持3 min后, 以10 ℃·min–1的速率升至270
℃, 保持5 min。MS (5975C型, Agilent Technologies
Company, Santa Clara, USA)工作条件: 电离方式:
EI; 电子能量为70 eV; 质量范围: 28–450 aum; 接
口温度280 ℃; 离子源温度为230 ℃; 四级杆温度
150 ℃。
1.4 数据分析
采用NIST2008谱库检索, 并根据已报道的植物
VOCs保留时间和特征离子对其各组分进行定性。
VOCs定量方法: 采用单位采样时间内单株植物释
放出的VOCs特征离子峰面积进行定量。使用
Oringin 8.0和SPSS软件进行数据处理、图表制作及
统计分析, 方差分析采用Duncan新复极差法。
2 结果和分析
2.1 干旱胁迫对渗透调节物质含量的影响
不同强度干旱胁迫处理对迷迭香叶片渗透调
节物质含量的影响存在明显差异(图1)。LD处理初期
与对照相比叶片可溶性糖和可溶性蛋白质含量无显
著差异, 处理24天时, 比对照分别提高了34.8%和
49.1% (p < 0.05)。
MD和SD处理, 迷迭香叶片可溶性糖含量均极
显著增加(p < 0.01) (图1A), 处理12天时, 叶片可溶
性糖含量比对照分别增加了51.5%和87.4%; 之后,
MD处理可溶性糖含量继续增加, SD处理可溶性糖
含量呈现下降趋势。可溶性蛋白质含量的变化趋势
与可溶性糖含量相似, MD和SD处理12天时, 可溶
性蛋白质含量均明显高于对照(图1B), 且达到极显
著水平(p < 0.01), 与对照相比分别提高了0.82倍和
1.40倍, MD随胁迫时间延长缓慢增加; SD处理可溶
性蛋白质含量呈现下降趋势。
刘芳等: 迷迭香对干旱胁迫的生理响应及其诱导挥发性有机化合物的释放 457

doi: 10.3724/SP.J.1258.2013.00047


图1 干旱胁迫对迷迭香渗透调节物质的影响(平均值±标准
偏差)。CK, 对照, 75%田间持水量; LD, 轻度干旱, 60%田间
持水量; MD, 中度干旱, 40%田间持水量; SD, 重度干旱,
20%田间持水量。
Fig. 1 Effects of drought stress on the osmotic adjustment
substances in Rosemarinus offcinalis (mean ± SD). CK, control,
75% field capacity; LD, light drought, 60% field capacity; MD,
middle drought, 40% field capacity; SD, severe drought, 20%
field capacity.


2.2 干旱胁迫对细胞膜的损伤
不同强度干旱胁迫处理后迷迭香叶片MDA含
量均呈现增加趋势(图2A), LD处理MDA含量增加
缓慢 , 处理24天时 , MDA含量增加了0.97倍(p <
0.01); 而MD和SD处理使MDA含量迅速增加, 并且
分别在处理8天和12天达到极显著水平(p < 0.01),
分别是对照的1.66倍和1.82倍, 随着干旱胁迫时间
的延长, MDA含量继续增加, 胁迫24天, MD和SD
处理迷迭香叶片MDA含量分别为对照的3.03倍和
3.58倍。随着干旱胁迫时间延长, 迷迭香叶片受伤
害程度逐渐增强(图2B), LD处理24天, 细胞膜受伤
害程度与对照无显著差异; MD处理24天, 细胞膜受
伤害程度增加了5.7%; SD处理12天, 细胞膜受伤害
程度达到最大值, 随着干旱胁迫时间延长, 细胞膜
受伤害程度无显著增加。


图2 干旱胁迫对迷迭香细胞的损伤(平均值±标准偏差)。
CK, 对照, 75%田间持水量; LD, 轻度干旱, 60%田间持水
量; MD, 中度干旱, 40%田间持水量; SD, 重度干旱, 20%田
间持水量。
Fig. 2 Effects of drought stress on cell injury in Rosemarinus
offcinalis (mean ± SD). CK, control, 75% field capacity; LD,
light drought, 60% field capacity; MD, middle drought, 40%
field capacity; SD, severe drought, 20% field capacity.


2.3 干旱胁迫对保护酶活性的影响
由图3可以看出, LD处理迷迭香叶片SOD、POD
和CAT活性与对照无显著差异。MD和SD处理随着
胁迫时间的延长, SOD活性逐渐增强(图3A), 分别
在处理的第12天和第8天达到最大值, 其SOD活性
分别比对照提高了25.9%和34.6% (p < 0.01); 随后
SOD活性迅速降低。干旱胁迫初期, MD和SD处理的
迷迭香POD和CAT活性与对照之间无显著差异(图
3B、3C); 随着胁迫时间的延长, MD和SD处理POD
活性逐渐增强, 处理到16天时, 与对照相比分别增
加了1.94倍和2.31倍(p < 0.01), 之后呈现下降的趋
势。CAT活性的变化与POD活性的变化基本相似(图
3C), MD和SD处理到16天时CAT活性达到最大值,
比对照增加了1.78倍和2.07倍。
2.4 干旱胁迫对LOX活性的影响
不同强度的干旱胁迫处理, 迷迭香LOX活性存
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图3 干旱胁迫对迷迭香保护酶活性的影响(平均值±标准偏
差)。CK, 对照, 75%田间持水量; LD, 轻度干旱, 60%田间持
水量; MD, 中度干旱, 40%田间持水量; SD, 重度干旱, 20%
田间持水量。CAT, 过氧化氢酶; POD, 过氧化物酶; SOD,
超氧化物歧化酶。
Fig. 3 Effects of drought stress on the activity of protective
enzymes in Rosemarinus offcinalis (mean ± SD). CK, control,
75% field capacity; LD, light drought, 60% field capacity; MD,
middle drought, 40% field capacity; SD, severe drought, 20%
field capacity. CAT, catalase; POD, peroxidase; SOD, super-
oxide dismutase.


在显著的差异(p < 0.05) (图4)。LD胁迫处理LOX活
性与对照无显著差异; MD和SD胁迫处理16天和12
天, LOX活性达到最大值, 与对照相比分别增加了
0.96和1.04倍(p < 0.01), 随后LOX活性呈现下降趋
势。
2.5 迷迭香释放VOCs成分分析
采用TDS/GC/MS联用技术对不同干旱胁迫处
理下迷迭香释放的VOCs成分进行分析, 共鉴定出
了59种化合物(表1)。随着干旱胁迫程度增加, 迷迭


图4 干旱胁迫对迷迭香脂氧合酶(LOX)活性的影响(平均值
±标准偏差)。CK, 对照, 75%田间持水量; LD, 轻度干旱,
60%田间持水量; MD, 中度干旱, 40%田间持水量; SD, 重
度干旱, 20%田间持水量。
Fig. 4 Effects of drought stress on lipoxygenase (LOX) activ-
ity in Rosemarinus offcinalis (mean ± SD). CK, control, 75%
field capacity; LD, light drought, 60% field capacity; MD,
middle drought, 40% field capacity; SD, severe drought, 20%
field capacity.


香释放的VOCs总量呈明显的下降趋势(图5), LD、
MD和SD分别比对照降低了0.8%、32.8%和57.0%,
同时诱导释放出10种新的VOCs成分。迷迭香萜烯
类和醛类化合物随着胁迫强度增加, 相对含量呈增
加的趋势, LD、MD和SD处理与对照相比萜烯类化
合物相对含量分别增加了14.4%、17.0%和23.7%,
同时新增加了三环烯、3-蒈烯和伞花烃; C6绿叶性气
体(green leaf volatiles, GLVs)和醛类化合物相对含
量分别增加了2.2%、0.9%和0.7%, 新增化合物有2-
己烯醛、叶醇、山梨醛和癸醛4种。迷迭香醇类、
酮类、酯类和醚类化合物的相对含量随着干旱程度
的加深而降低。
3 讨论和结论
植物对逆境的反应是一个复杂的响应机制。现
有研究表明, 干旱胁迫下, 很多植物通过主动积累
可溶性有机溶质或无机离子来改善植物叶片的水
分状况和维持细胞膨压, 为其正常生命活动创造条
件(Farooq, 2009, 2010; 金雅琴等, 2012), 而且可溶
性物质积累量越高, 抗旱性越强(Chaves & Oliveira,
2004; Ashraf & Iram, 2005), 但严重干旱时可溶性
物质积累量可能下降(Pinheiro et al., 2001; Patakas
刘芳等: 迷迭香对干旱胁迫的生理响应及其诱导挥发性有机化合物的释放 459

doi: 10.3724/SP.J.1258.2013.00047
表1 迷迭香挥发性有机化合物的主要成分(平均值±标准偏差)
Table 1 Main components of the volatile organic compounds from Rosemarinus offcinalis (mean ± SD)
峰面积×106
Peak area ×106
保留时间
Retention time
(min)
挥发性有机化合物
Volatile organic compounds
分子式
Chemical
formula 对照
Control
轻度干旱
Light drought
中度干旱
Intermediate drought
重度干旱
Severe drought
5.18 3-己烯-2-酮 3-Hene-2-one C6H10O 2.58 ± 0.21 8.93 ± 0.32 5.63 ± 0.12 1.46 ± 0.03
6.66 2-己烯醛 (E)-2-Hexenal C6H10O – – 1.07 ± 0.08 1.14 ± 0.13
6.78 叶醇 Leaf alcohol C6H12O – 1.12 ± 0.18 1.22 ± 0.05 0.93 ± 0.07
7.42 α-蒎烯 α-Pinene C10H16 3.95 ± 0.02 0.81 ± 0.01 3.98 ± 0.12 1.73 ± 0.10
8.19 山梨醛 Sorbaldehyde C6H8O – – – 0.53 ± 0.01
8.47 三环烯 Tricyclene C10H16 – – 0.59 ± 0.03 0.77 ± 0.02
8.69 侧柏烯 Thujene C10H16 10.08 ± 1.19 8.06 ± 0.91 6.92 ± 0.92 6.27 ± 0.87
8.91 β-蒎烯 β-Pinene C10H16 83.18 ± 3.83 50.75 ± 4.61 76.62 ± 8.12 79.43 ± 7.31
9.24 樟烯 Camphene C10H16 17.52 ± 1.09 9.19 ± 0.99 17.10 ± 2.12 15.76 ± 1.12
9.39 伞柳醇 Umbellulol C10H16O 13.02 ± 1.92 15.75 ± 1.18 10.04 ± 1.03 6.83 ± 1.76
10.00 桧烯 Sabinene C10H16 16.10 ± 2.29 9.92 ± 1.22 14.90 ± 2.01 13.00 ± 1.89
10.52 月桂烯 Myrcene C10H16 52.20 ± 5.05 55.83 ± 5.42 27.37 ± 2.19 15.43 ± 1.23
10.80 水芹烯 Phellandrene C10H16 19.72 ± 1.11 18.23 ± 1.83 9.15 ± 1.21 4.84 ± 0.58
10.88 3-蒈烯 3-Carene C10H16 – – 1.23 ± 0.05 0.82 ± 0.02
11.12 α-萜品烯 α-Terpinene C10H16 24.81 ± 2.07 22.30 ± 3.05 11.09 ± 0.98 5.72 ± 1.33
11.37 伞花烃 o-Cymene C10H14 – 97.67 ± 9.11 57.32 ± 3.47 20.21 ± 1.34
11.56 α-萜品醇 α-Terpineol C10H18O 100.80 ± 9.89 8.12 ± 0.88 1.12 ± 0.21 21.63 ± 1.68
11.99 罗勒烯 Ocimene C10H16 5.02 ± 0.89 12.12 ± 1.31 6.62 ± 0.67 3.65 ± 0.45
12.35 β-萜品烯 β-Terpinene C10H16 52.54 ± 3.89 55.04 ± 3.78 20.59 ± 1.95 10.88 ± 1.04
13.08 萜品油烯 Terpinolene C10H12 33.99 ± 2.87 34.61 ± 3.01 15.72 ± 1.03 8.24 ± 0.56
13.44 里那醇 Linalool C10H18O 33.40 ± 3.68 31.12 ± 2.93 16.48 ± 1.92 6.33 ± 0.74
13.59 蒿萜酮 Eucarvone C9H16O 3.56 ± 0.23 2.34 ± 0.05 1.78 ± 0.17 0.45 ± 0.02
14.07 菊油环酮 Chrysanthenone C10H14O 41.42 ± 4.56 30.60 ± 3.32 18.04 ± 1.05 6.57 ± 0.21
14.39 松香芹醇 Pinocarveol C10H16O 1.16 ± 0.06 1.86 ± 0.06 1.52 ± 0.12 0.64 ± 0.06
14.53 樟脑 Camphor C10H16O 28.11 ± 2.78 20.78 ± 2.01 21.29 ± 3.02 8.24 ± 0.93
14.74 异龙脑 Isoborneol C10H18O 0.58 ± 0.03 0.58 ± 0.01 0.74 ± 0.01 21.04 ± 2.03
14.93 松香芹酮 Pinocarvone C10H14O 2.21 ± 0.09 4.90 ± 0.08 3.50 ± 0.01 1.31 ± 0.02
15.21 龙脑 Borneol C10H18O 46.85 ± 5.03 41.58 ± 4.18 49.85 ± 5.01 2.93 ± 0.09
15.28 松莰酮 Pinocamphone C10H16O 4.35 ± 0.54 1.18 ± 0.03 3.32 ± 0.02 3.06 ± 0.02
15.34 4-萜品醇 4-Carvomenthenol C10H18O 11.29 ± 1.09 12.97 ± 1.21 8.30 ± 0.80 8.69 ± 0.60
15.64 2-蒎烯-4-酮 2-Pinen-4-one C10H14O 1.13 ± 0.03 – 0.94 ± 0.02 2.98 ± 0.21
15.81 草蒿脑 Estragole C10H12O – – 2.12 ± 0.22 3.36 ± 0.28
15.87 顺式萜品醇 cis-Terpineol C10H18O 18.07 ± 1.09 14.62 ± 0.12 9.49 ± 0.08 –
16.03 癸醛 Decanal C10H20O – – 1.38 ± 0.11 –
16.06 桃金娘烯醇 Myrtenol C10H16O 3.28 ± 0.28 5.14 ± 0.34 1.69 ± 0.14 –
16.28 反式马鞭草烯酮 trans-Verbenone C10H14O 25.61 ± 2.77 25.22 ± 3.21 36.43 ± 3.98 22.07 ± 2.32
16.33 2-烯丙基-4-甲基苯酚 2-Allyl-4-methylphenol C10H12O – – 0.95 ± 0.04 3.36 ± 0.29
16.77 香茅醇 Citronellol C10H20O 2.22 ± 0.11 2.89 ± 0.29 1.26 ± 0.07 0.83 ± 0.03
17.08 蒈醇 Caranol C10H18O 1.83 ± 0.01 1.33 ± 0.04 1.00 ± 0.01 –
17.29 桃金娘烷醇 Myrtanol C10H16O 4.35 ± 0.37 4.17 ± 0.34 2.88 ± 0.17 –
17.70 香叶醇 Lemonol C10H18O 8.72 ± 1.06 12.97 ± 1.29 4.63 ± 0.38 2.06 ± 0.14
18.27 柠檬醛 Citral C10H16O 3.67 ± 0.32 18.11 ± 1.22 2.38 ± 0.19 0.88 ± 0.02
18.34 香芹酮 Carvone C10H14O 3.45 ± 0.29 – 3.06 ± 0.32 2.43 ± 0.33

460 植物生态学报 Chinese Journal of Plant Ecology 2013, 37 (5): 454–463

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表1 (续) Table 1 (continued)
峰面积×106
Peak area ×106
保留时间
Retention time
(min)
挥发性有机化合物
Volatile organic compounds
分子式
Chemical
formula 对照
Control
轻度干旱
Light drought
中度干旱
Intermediate drought
重度干旱
Severe drought
18.41 菊酸甲酯 Methyl chrysanthemate C11H18O2 1.49 ± 0.16 4.10 ± 1.06 1.37 ± 0.11 0.58 ± 0.01
18.87 乙酸龙脑酯 Bornyl acetate C12H10O2 46.21 ± 6.21 73.16 ± 5.98 23.67 ± 2.11 14.77 ± 1.88
19.06 菊酸乙酯 Hrysanthenyl acetate C12H18O2 0.77 ± 0.01 1.36 ± 0.01 1.07 ± 0.01 –
20.06 乙酸桃金娘烯酯 Myrtenyl acetate C12H18O2 1.52 ± 0.07 2.88 ± 0.09 0.67 ± 0.02 –
20.35 冰片烯 Bornylene C10H16 1.34 ± 0.13 3.09 ± 0.41 1.32 ± 0.06 0.51 ± 0.01
20.90 香茅醇乙酸酯 Citronellyl acetate C10H18 0.51 ± 0.04 7.03 ± 0.76 0.45 ± 0.01 –
21.23 乙酸异洋薄荷酯 Sopulegol acetate C10H18O 3.46 ± 0.65 1.67 ± 0.03 0.64 ± 0.03 0.43 ± 0.06
21.82 乙酸香叶酯 Geraniol acetate C10H14O 2.75 ± 0.03 2.90 ± 0.03 0.94 ± 0.04 –
22.20 顺式马鞭草烯酮 cis-Verbenone C10H14O 10.89 ± 1.03 7.71 ± 0.67 5.38 ± 0.56 0.75 ± 0.02
22.46 丁香油酚甲醚 Eugenol methyl ether C11H14O2 9.91 ± 1.12 14.27 ± 1.21 5.41 ± 0.34 3.16 ± 0.23
22.93 反式石竹烯 trans-Caryophyllene C15H24 46.61 ± 4.07 40.74 ± 3.75 21.11 ± 1.95 8.43 ± 0.94
23.64 香叶基丙酮 Dihydropseudoionon C13H22O 1.40 ± 0.01 1.11 ± 0.02 0.96 ± 0.08 –
23.72 顺式石竹烯 cis-Caryophyllene C15H24 6.99 ± 0.72 6.31 ± 0.65 2.95 ± 0.02 1.20 ± 0.03
24.75 十五烷 Hexadecane C16H34 – 1.00 ± 0.01 0.49 ± 0.01 0.45 ± 0.02
26.67 氧化石竹烯 Caryophyllene oxide C11H14O2 0.72 ± 0.03 – – –
26.77 揽香烯 Elemene C15H24 0.54 ± 0.02 – – –
–, 未检测到化合物。
–, no compound is found.


et al., 2002)。本研究表明, 在MD胁迫下, 迷迭香叶
片通过增加体内可溶性糖和可溶性蛋白含量(图1),
调节体内水分平衡来维持正常的代谢; 在SD胁迫
条件下, 随干旱胁迫时间的延长, 两类渗透调节物
质含量先升高后降低, 表现出较强的渗透调节能
力。膜系统通常被认为是干旱伤害的关键部位。干
旱胁迫诱导大量的活性氧(reactive oxygen species,
ROS)产生, 破坏了植物内部的平衡(Apel & Hirt,
2004; Jaspers & Kangasjävi, 2010)。在此过程中, 植
物通过调动保护酶来清除体内ROS。但是调动保护
酶的能力是有限的, 在超出了植物的忍耐范围后,
保护酶活性迅速下降, 造成了细胞膜脂过氧化的加
剧, 使细胞膜通透性增大(Apel & Hirt, 2004 )。膜脂
过氧化导致植物体内MDA大量生成, 引起植物细
胞蛋白质和核酸等生命大分子交联聚合, 进一步对
植物细胞造成毒害(高悦等, 2012; 文瑛等, 2012)。
本研究表明, 随着干旱胁迫程度的加强, 迷迭香叶
片的MDA含量和相对电导率升高, 与胁迫强度和
时间呈显著正相关(图2), 说明在干旱胁迫下, 植物
代谢紊乱发生膜脂过氧化, 质膜遭到损伤, 大量离
子外渗, MDA积累。SOD、POD和CAT是细胞内清
除活性氧的主要保护酶, 对活性氧的清除能力是决
定细胞抗逆性大小的关键因素, 保护酶系统的防御
能力取决于这几种酶彼此协调的综合结果(Jaspers
& Kangasjävi, 2010; Vaahtera & Brosché, 2011)。本
研究表明, 在不同程度干旱胁迫下, 迷迭香叶片3
种保护酶活性的变化规律有所不同(图3)。在MD胁
迫和SD胁迫初期, 迷迭香体内产生了大量ROS, 致
使保护酶活性增加, 由SOD歧化超氧阴离子产生的
H2O2也必然增多, POD和CAT活性也有所增加, 说
明迷迭香体内3种保护酶开始对干旱胁迫作出响应;
随着胁迫时间的延长, 迷迭香体内的代谢趋于混
乱, SOD活性开始下降。而清除H2O2的CAT和POD
活性继续升高, 胁迫到20天时才开始下降, 表明这
3种酶对干旱胁迫的响应可能存在一定差异, 表现
为相互协调的作用。
众多研究表明, 植物各种组织中产生广泛的
VOCs, 具有直接和间接的信号调控作用(Dudareva,
et al., 2004; Laothawornkitkul et al., 2008; 左照江
等, 2010)。最近研究发现, 植物释放的VOCs在抵抗
环境胁迫中也发挥着重要作用(Blanch et al., 2007;
Gershenzon & Dudareva, 2007; Staudt et al., 2008;
Grote et al., 2009; Ibrahim et al., 2010; Loreto &
Schnitzler, 2010)。本研究表明, LD处理迷迭香萜烯
刘芳等: 迷迭香对干旱胁迫的生理响应及其诱导挥发性有机化合物的释放 461

doi: 10.3724/SP.J.1258.2013.00047


图5 干旱胁迫下迷迭香挥发性有机化合物的总离子流图。
A, 峰面积; CK, 对照, 75%田间持水量; LD, 轻度干旱, 60%
田间持水量; MD, 中度干旱, 40%田间持水量; SD, 重度干
旱, 20%田间持水量。
Fig. 5 Total ion current of volatile organic compounds
(VOCs) of Rosemarinus offcinalis under drought stresses. A,
peak area; CK, control, 75% field capacity; LD, light drought,
60% field capacity; MD, middle drought, 40% field capacity;
SD, severe drought, 20% field capacity.

类化合物释放量显著高于对照(表1), 说明轻度干旱
能够诱导迷迭香大量释放萜烯类化合物, 改善胁迫
造成的对氧化反应的应激保护(Loreto & Schnitzler,
2010); MD和SD处理迷迭香释放萜烯类总量与对照
相比减少(表1), 一方面是因为干旱诱导气孔关闭,
抑制了VOCs通过气孔途径向外界排放(Niinemets,
2004); 另一方面, 由于干旱胁迫使光合作用受到抑
制, 光合产物总量降低, 供应到2-C-甲基-D-赤藓糖
醇-4-磷酸合成途径(MEP)合成萜烯类挥发物的碳源
也会相应降低(Loreto & Schnitzler, 2010; Simpraga
et al., 2011)。随着干旱胁迫程度的加深, 单萜类相
对含量呈现明显的增加趋势(表1), 可能是由于分配
到MEP途径中合成单萜的碳源比例增加。Simpraga
(2011)等研究发现, 干旱胁迫过程中, 单萜化合物
释放量与净光合产量之比随着干旱程度的加深呈
现增加的趋势, 单萜化合物释放量的增加能够减少
有害自由基的累积 , 减轻叶绿体膜的氧化损伤
(Delfine et al., 2005)。
GLVs是氧化多烯脂肪酸(polyenoic fatty acids,
PUFA)的衍生物, 由LOX催化具有顺,顺-1,4-戊二烯
结构的不饱和脂肪酸进行加氧反应生成的含氧
VOCs (Loreto & Schnitzler, 2010)。SOD、POD和CAT
清除ROS的能力是有限的, 干旱胁迫后期, 大量累
积的ROS会破坏植物细胞膜结构, 进而诱导LOX活
性增强 , 催化不饱和脂肪酸形成大量的GLVs
(Holopainen & Gershenzon, 2010)。本研究发现, 随
着干旱胁迫时间延长, LOX活性均呈现先增加后降
低的趋势 (图4), 干旱胁迫后 , 从迷迭香释放的
VOCs中新检测到了2-己烯醛、叶醇、山梨醛和癸醛
等4种化合物 , 新物质的产生与干旱胁迫过程中
LOX活性升高呈现正相关(Holopainen & Gershen-
zon, 2010)。
综上所述, LD胁迫条件下, 迷迭香主要通过提
高渗透调节物质含量和释放萜烯类化合物抵抗干
旱胁迫; MD和SD胁迫初期, 迷迭香通过提高保护
酶活性来降低ROS对细胞膜的损伤; 长时间SD胁
迫会导致迷迭香代谢紊乱, SOD活性下降, 诱导迷
迭香LOX酶活性增加, 催化细胞内游离脂肪酸大量
合成GLVs及醛类VOCs, 减少ROS的累积, 减轻叶
绿体膜氧化的损伤, 提高迷迭香的抗旱性。
基金项目 国家自然基金(30972397和31270756)和
浙江农林大学科研发展基金(2010FR058)。
参考文献
Apel K, Hirt H (2004). Reactive oxygen species: metabolism,
oxidative stress, and signal transduction. Annual Review of
Plant Biology, 55, 373–399.
Ashraf M, Iram A (2005). Drought stress induced changes in
some organic substances in nodules and other plant parts
of two potential legumes differing in salt tolerance.
Flora-Morphology, Distribution, Functional Ecology of
Plants, 200, 535–546.
Atkinson NJ, Urwin PE (2012). The interaction of plant biotic
and abiotic stresses: from genes to the field. Journal of
Experimental Botany, 63, 3523–3543.
Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston
CA (2006). Volatile signaling in plant-plant interactions:
“Talking trees” in the genomics era. Science, 311, 812–
815.
Bengough AG, McKenzie BM, Hallett PD, Valentine TA
(2011). Root elongation, water stress, and mechanical im-
pedance: a review of limiting stresses and beneficial root
462 植物生态学报 Chinese Journal of Plant Ecology 2013, 37 (5): 454–463

www.plant-ecology.com
tip traits. Journal of Experimental Botany, 62, 59–68.
Blanch JS, Peñuelas J, Llusià J (2007). Sensitivity of terpene
emissions to drought and fertilization in terpene-storing
Pinus halepensis and non-storing Quercus ilex. Physiolo-
gia Plantarum, 131, 211–225.
Bradford MM (1976). A rapid and sensitive method for the
quantitation of microgram quantities of protein utilizing
the principle of protein-dye binding. Analytical Biochem-
istry, 72, 248–254.
Chance B, Maehly AC (1955). Assay of catalase and peroxi-
dase. Methods in Enzymology, 2, 764–775.
Chaves MM, Oliveira MM (2004). Mechanisms underlying
plant resilience to water deficits: prospects for water- sav-
ing agriculture. Journal of Experimental Botany, 55,
2365–2384.
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K
(2011). Effects of abiotic stress on plants: a systems biol-
ogy perspective. BMC Plant Biology, 11, 163.
Delfine S, Loreto F, Pinelli P, Tognetti R, Alvino A (2005).
Isoprenoids content and photosynthetic limitations in
rosemary and spearmint plants under water stress. Agri-
culture, Ecosystems & Environment, 106, 243–252.
Dicke M, Loreto F (2010). Induced plant volatiles: from genes
to climate change. Trends in Plant Sciences, 15, 115–117.
Dudareva N, Pichersky E, Gershenzon J (2004). Biochemistry
of plant volatiles. Plant Physiology, 135, 1893–1902.
Farooq M, Wahid A, Ahmad N, Asad SA (2010). Comparative
efficacy of surface drying and re-drying seed priming in
rice: changes in emergence, seedling growth and associa-
ted metabolic events. Paddy and Water Environment, 8,
15–22.
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA
(2009). Plant drought stress: effects, mechanisms and
management. Agronomy for Sustainable Development, 29,
185–212.
Filella I, Peñuelas J, Seco R (2009). Short-chained oxygenated
VOC emissions in Pinus halepensis in response to
changes in water availability. Acta Physiologiae Planta-
rum, 31, 311–318.
Gao Y, Jin YJ, Li HD, Chen HJ (2005). Volatile organic com-
pounds and their roles in bacteriostasis in five conifer spe-
cies. Journal of Integrative Plant Biology, 47, 499–507.
Gao Y, Zhu YZ, Yang ZM, Du HM (2012). Effects of drought
stress and recovery on antioxidant enzyme activities of
Agropyron cristatum. Acta Agrectir Sinica, 20, 336–341.
(in Chinese with English abstract) [高悦, 朱永铸, 杨志
民, 杜红梅 (2012). 干旱胁迫和复水对冰草相关抗性
生理指标的影响. 草地学报, 20, 336–341. ]
Gershenzon J, Dudareva N (2007). The function of terpene
natural products in the natural world. Nature Chemical
Biology, 3, 408–414.
Giannopolitis CN, Ries SK (1977). Superoxide dismutase: I.
Occurrence in higher plants. Plant Physiology, 59,
309–314.
Gill SS, Tuteja N (2010). Reactive oxygen species and anti-
oxidant machinery in abiotic stress tolerance in crop
plants. Plant Physiology and Biochemistry, 48, 909–930.
Gouinguené SP, Turlings TCJ (2002). The effects of abiotic
factors on induced volatile emissions in corn plants. Plant
Physiology, 129, 1296–1307.
Grote R, Lavoir AV, Rambal S, Staudt M, Zimmer I, Schnitzler
JP (2009). Modelling the drought impact on monoterpene
fluxes from an evergreen Mediterranean forest canopy.
Oecologia, 160, 213–223.
Grote R, Keenan T, Lavoir AV, Staudt M (2010). Process-
based simulation of seasonality and drought stress in
monoterpene emission models. Biogeosciences, 7, 257–
274.
Hatanaka A (1993). The biogeneration of green odour by green
leaves. Phytochemistry, 34, 1201–1218.
Holopainen JK, Gershenzon J (2010). Multiple stress factors
and the emission of plant VOCs. Trends in Plant Science,
15, 176–184.
Huang HM, Guo ZJ, Lu RM, Meng L (2012). Optimization of
extraction technology of volatile oil from rosemary and
analysis on the chemical constituents of volatile oil. Hubei
Agricultural Sciences, 51, 2321–2324. (in Chinese with
English abstract) [黄宏妙 , 郭占京 , 卢汝梅 , 蒙亮
(2012). 迷迭香挥发油提取工艺优化及其化学成分分
析. 湖北农业科学, 51, 2321–2324.]
Ibrahim MA, Maenpaa M, Hassinen V, Kontunen-Soppela S,
Malec L, Rousi M, Pietikainen L, Tervahauta A,
Karenlampi S, Holopainen JK, Oksanen EJ (2010).
Elevation of night-time temperature increases terpenoid
emissions from Betula pendula and Populus tremula.
Journal of Experimental Botany, 61, 1583–1595.
Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ,
Somasundaram R, Vam RP (2009). Drought stress in
plants: a review on morphological characteristics and
pigments composition. International Journal of
Agriculture and Biology, 11, 100–105.
Jaspers P, Kangasjärvi J (2010). Reactive oxygen species in
abiotic stress signaling. Physiologia Plantarum, 138,
405–413.
Jin YQ, Li DL, Chen XX, Zhang LJ (2012). Physiological re-
sponse of Sapium sebiferum seedlings from different
provenances to drought stress. Acta Botanica Boreali-
Occidentalia Sinica, 32, 1395–1402. (in Chinese with
English abstract) [金雅琴 , 李冬林 , 陈小霞 , 张丽娟
(2012). 不同种源乌桕幼苗对干旱胁迫的生理响应. 西
北植物学报, 32, 1395–1402.]
Laothawornkitkul J, Paul ND, Vickers CE, Possell M, Taylor
JE, Mullineaux PM, Hewitt CN (2008). Isoprene
emissions influence herbivore feeding decisions. Plant,
Cell & Environment, 31, 1410–1415.
Lavoir AV, Staudt M, Schnitzler JP, Landais D, Massol F,
刘芳等: 迷迭香对干旱胁迫的生理响应及其诱导挥发性有机化合物的释放 463

doi: 10.3724/SP.J.1258.2013.00047
Rocheteau A, Rodriguez R, Zimmer I, Rambal S (2009).
Drought reduced monoterpene emissions from Quercus
ilex trees: results from a throughfall displacement experi-
ment within a forest ecosystem. Biogeosciences Discus-
sions, 6, 863–893.
Loreto F, Schnitzler JP (2010). Abiotic stresses and induced
BVOCs. Trends in Plant Science, 15, 154–166.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010). Reac-
tive oxygen species homeostasis and signalling during
drought and salinity stresses. Plant, Cell & Environment,
33, 453–467.
Niinemets U, Loreto F, Reichstein M (2004). Physiological and
physicochemical controls on foliar volatile organic com-
pound emissions. Trends in Plant Science, 9, 180–186.
Patakas A, Nikolaou N, Zioziou E, Radoglou K, Noitsakis B
(2002). The role of organic solute and ion accumulation in
osmotic adjustment in drought-stressed grapevines. Plant
Science, 163, 361–367.
Pinheiro C, Chaves MM, Ricardo CP (2001). Alterations in
carbon and nitrogen metabolism induced by water deficit
in the stems and leaves of Lupinus albus L. Journal of
Experimental Botany, 52, 1063–1070.
Potters G, Pasternak TP, Guisez Y, Jansen MAK (2009). Dif-
ferent stresses, similar morphogenic responses: integrating
a plethora of pathways. Plant, Cell & Environment, 32,
158–169.
Simpraga M, Verbeeck H, Demarcke M, Joó É, Pokorska O,
Amelynck C, Schoon N, Dewulf J, van Langenhove H,
Heinesch B, Aubinet M, Laffineur Q, Müller JF, Steppe K
(2011). Clear link between drought stress, photosynthesis
and biogenic volatile organic compounds in Fagus sylva-
tica L. Atmospheric Environment, 45, 5254–5259.
Staudt M, Ennajah A, Mouillot F, Joffre R (2008). Do volatile
organic compound emissions of Tunisian cork oak popu-
lations originating from contrasting climatic conditions
differ in their responses to summer drought? Canadian
Journal of Forest Research, 38, 2965–2975.
Sui XY, Liu TT, Ma CH, Yang Z, Zu YG, Zhang L, Wang H
(2012). Microwave irradiation to pretreat rosemary (Ros-
marinus officinalis L.) for maintaining antioxidant content
during storage and to extract essential oil simultaneously.
Food Chemistry, 131, 1399–1405.
Tai J, Cheung S, Wu M, Hasman D (2012). Antiproliferation
effect of rosemary (Rosmarinus officinalis) on human
ovarian cancer cells in vitro. Phytomedicine, 19, 436–443.
Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H (2010).
Cold stress effects on reproductive development in grain
crops: an overview. Environmental and Experimental
Botany, 67, 429–443.
Vaahtera L, Brosché M (2011). More than the sum of its
parts-how to achieve a specific transcriptional response to
abiotic stress. Plant Science, 180, 421–430.
Wang H, Gao HY, Zhang ZQ, Wu LJ (2011). Isolation and
identification of chemical constituents from Rosmarinus
officinalis L. Modern Chinese Medicine, 13(1), 23–25. (in
Chinese with English abstract) [王珲, 高慧媛, 张振秋,
吴立军 (2011). 中药迷迭香化学成分的分离与鉴定.
中国现代中药, 13(1), 23–25.]
Wen Y, Liao FY, Liu ZH (2012). The Effect of water stress on
the physiology of Sophora japonica ‘Golden stem’. Chi-
nese Agricultural Science Bulletin, 28(13), 47–52. (in
Chinese with English abstract) [文瑛, 廖飞勇, 刘智慧
(2012). 不同水分胁迫对黄枝槐生理特性的影响研究.
中国农学通报, 28(13), 47–52.]
Yuan GJ, Li PB, Yang H (2012). Anti-MRSA activity of car-
nosic acid in rosemary. Chinese Journal of Modern Ap-
plied Pharmacy, 29, 571–574. (in Chinese with English
abstract) [袁干军, 李沛波, 杨慧 (2012). 迷迭香中鼠尾
草酸的抗MRSA活性研究 . 中国现代应用药学 , 29,
571–574.]
Zhang JX, Kirkham MB (1994). Drought stress induced
changes in activities of superoxide dismutase, catalase,
and peroxidase in wheat species. Plant and Cell Physiol-
ogy, 35, 785–791.
Zhang XF, Kong HY, Li PF, Li JN, Xiong JL, Wang SM,
Xiong YC (2011). Recent advances in research on drought
induced proteins and the related genes in wheat (Triticum
aestivu L.). Acta Ecologica Sinica, 31, 2641–2653. (in
Chinese with English abstract) [张小丰, 孔海燕, 李朴芳,
李冀南, 熊俊兰, 王绍明, 熊友才 (2011). 小麦干旱诱
导蛋白及相关基因研究进展 . 生态学报 , 31, 2641–
2653.]
Zhou S, Lin FP, Wang YK, Shen YB, Zhang RM, Gao RF, Gao
Y (2012). Effects of mechanical damage of leaves on
volatile organic compounds and chlorophyll fluorescence
parameters in seedlings of Cinnamomum camphora. Chi-
nese Journal of Plant Ecology, 36, 671–680. (in Chinese
with English abstract) [周帅, 林富平, 王玉魁, 沈应柏,
张汝民, 高荣孚, 高岩 (2012). 樟树幼苗机械损伤叶片
对挥发性有机化合物及叶绿素荧光参数的影响. 植物
生态学报, 36, 671–680.]
Zuo ZJ, Zhang RM, Wang Y, Hou P, Wen GS, Gao Y (2010).
Analysis of main volatile organic compounds and study of
aboveground structures in Artemisia frigida. Chinese
Journal of Plant Ecology, 34, 462–468. (in Chinese with
English abstract) [左照江, 张汝民, 王勇, 侯平, 温国胜,
高岩 (2010). 冷蒿挥发性有机化合物主要成分分析及
其地上部分结构研究. 植物生态学报, 34, 462–468.]

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