全 文 ：夜间低温对生长在两种光强下两个芒果品种的
气体交换和叶绿素荧光的影响
?
Nabil I . ELSHEERY1 ,2 , Burkhard WILSKE1 , 曹坤芳1
??
(1 中国科学院西双版纳热带植物园 , 云南 勐腊 666303 ; 2 中国科学院研究生院 , 北京 100049)
摘要 : 研究了夜间低温对两个芒果 ( Mangifera indica) 品种翡翠芒 (Khieo Sawoei ) 和四季芒 ( Choke Anand)
光合生理的影响。两个芒果品种的幼苗盆栽于全光和 50%相对光强下一年。在第二年的冬季 , 连续 7 天晚
上将芒果幼苗移到 4℃的冷库中 , 白天保持原条件。于低温处理前、处理期间和结束低温处理后 10 天中测
定芒果幼苗的光合生理特征。结果表明 , 夜间低温导致两个芒果品种的净光合速率、气孔导度和光系统 II
的最大光化学效率 ( Fv?Fm) 降低、非光化学猝灭 (NPQ) 上升。夜间低温对生长在全光下的芒果幼苗光
合作用的抑制比 50 %光下的更重。翡翠芒的 Fv?Fm 比四季芒下降的更多 , 但后者的 NPQ 上升更多。夜间
低温还导致两种光下芒果幼苗叶片的叶绿素含量下降 , 类胡萝卜素?叶绿素比值、丙二醛含量、膜的透性
和可溶性化合物 (可溶性总糖和脯氨酸 ) 上升。解除低温胁迫后 , 四季芒 Fv?Fm 的恢复比翡翠芒的快。
解除低温胁迫 7 天后二者的 Fv?Fm 能完全恢复。上述结果表明 , 翡翠芒对低温更敏感 , 遮荫可以明显缓解
两个芒果品种低温引起的光抑制。
关键词 : 叶绿素荧光 ; 气体交换 ; 芒果 ; 膜脂过氧化 ; 夜间低温 ; 渗透调节
中图分类号 : Q 945 文献标识码 : A 文章编号 : 0253 - 2700 (2008) 04 - 447 - 10
The Effect of Night Chilling on Gas Exchange and Chlorophyll
Fluorescence of Two Mango Cultivars Growing
under Two Irradiances
Nabil I . ELSHEERY1 , 2 , Burkhard WILSKE1 , CAO Kun-Fang1 **
(1 Xishuangbanna Tropical Botanical Garden, ChineseAcademy of Sciences, Mengla 666303 , China;
2 GraduateUniversity of Chinese Academy of Sciences, Beijing 100049 , China)
Abstract : Weinvestigated theeffect of night chillingon thephotosynthetic physiologyof two cultivars of mango ( Mangifera
indica)‘Choke Anand’and‘Khieo Sawoei’. The pottedmango seedlings of both cultivarsweregrown under thefull light
and 50% daylight for one year . In the following winter season (February 2006) , the seedlingsweremoved to a cold stor-
age roommaintaining 4℃ for seven consecutivenights and returned to their original places duringthe rest of theday . Pho-
tosynthetic physiologywasmeasuredbefore, duringthetreatment, and during10 days after thetreatment . Chill-night treat-
ment resulted in strong suppression in net photosynthesis ( Pn ) , stomatal conductance ( gs ) , andmaximumphotochemical
efficiency of PSII ( Fv?Fm ) , and increased non-photochemical quenching (NPQ) for both cultivars . Overall , the chilling-
induced photosynthetic suppression was stronger in seedlings grown in full sunlight than in50 % daylight . The decrease in
Fv?Fm was stronger in‘Khieo Sawoei’than in‘Choke Anand’cultivar, and the increase of NPQ was relatively higher in
‘Choke Anand’compared to‘Khieo Sawoei’cultivar . Night chilling resulted in a decrease in chlorophyll content and in-
云 南 植 物 研 究 2008 , 30 (4) : 447～456
Acta Botanica Yunnanica DOI : 10 .3724?SP. J . 1143 .2008.07260
?
?? ?Author for correspondence; E-mail : caokf@ xtbg. ac. cn
Received date: 2007 - 11 - 05 , Accepted date: 2008 - 02 - 02
作者简介 : Nabil Elsherry (1970 - ) 男 , 在读博士研究生 , 讲师 , 主要从事植物生理生态学研究。 ?
Foundation item: The National Natural Science Foundation of China ( 90302013 )
crease in thecarotenoid: chlorophyll ratios, themalondialdehyde (MDA) contents, membrane leakage, aswell as compat-
ible solutes ( total soluble sugar and proline) under both irradiances . After terminationof the chilling treatment, the recov-
ery of Fv?Fm was relatively quicker in‘Choke Anand’than in‘Khieo Sawoei’cultivar . Bothcultivars showed a complete
recovery after seven days of termination of thechilling treatment . These results showedthat‘KhieoSawoei’wasmore sen-
sitive to chilling than‘Choke Anand’, and shading significantly alleviated the chilling-induced photoinhibition .
Key words: Chlorophyll fluorescence; Gas exchange; Mango; Membrane lipid peroxidation; Night chilling; Osmotic ad-
justment
Low temperature is amajor factor limitingthe pro-
ductivity and geographical distribution of many plant
species . Chilling, non-freezing, temperatures can
cause injury for many tropical and subtropical plants,
including important fruit trees such as mango (Graham
and Patterson, 1982) . Mango occupies third place in
total Worldproductionof major tropical fruit crops after
citrus, and banana (Alonso and Blaikie, 2003) . Chi-
na is the second-largest producerof mango in theWorld
(FAO, 2002) . Oneof themajor areasof growing trop-
ical crops including mango is the southern Yunnan
Province, which is located at thenorthernborder of the
tropics . In thewet tropics, plants includingmango grow
all year round, when introduced to the marginal areas
they are vulnerable to chilling temperatures ( Greer,
1990; Ortiz-Lopez et al. , 1990; Cao et al. , 2006) .
Strong coldwinds coming fromnorthernChina oc-
casionally hit the southern Yunnan, with the extreme
temperature down to 2℃ in the lowland and alongwith
the clear-sky condition . Even in a normal winter, the
temperature in the lowland can go down to about 6℃ .
In thestudyareaXishuangbanna, extreme chilling tem-
peratures can cause severe injury and even death of
tropical crops such as mango, coffee, and rubber tree
(Hong and Li , 2001 ) . Exposure to chilling tempera-
tures results in suppression in the activities of photo-
synthetic enzymes, increase in stomatal limitation, and
therefore reduction in photosynthesis of tropical plants
(Nir et al. , 1997; Flexas et al. , 1999; Allen et al. ,
2000; Guo andCao, 2004) . Further effects of chilling
temperatures include a decreaseof root functioning and
water transport of xylem because of low soil tempera-
tures, which in turn induce further reduction in stoma-
tal conductance and thus leaf transpiration ( Hallgren
and Oquest, 1990) .
Under the clear-sky conditions, suppression of
photosynthesis leads to excess light energy in the chlo-
roplasts and consequently photoinhibition and photoxi-
dation ( Demmig-Adams and Adams, 1992; Chow,
1994) . Chronic photoinhibition in mango as indicated
by sustained reduction of maximum quantum efficiency
of PSII photochemistry ( Fv?Fm ) was reported during
the Israeli winter, which was correlated with the previ-
ous minimum night air temperature (Nir et al. , 1997;
Allen et al. , 2000) . Under this photoinhibitory condi-
tions, protective thermal dissipation occurs, mainly by
the formation of a trans-thylakoid of pH gradient
(Krause and Behrend, 1986) and through the xantho-
phyll cycle (Demmig-Adams, 1990) . These processes
enable the plants to balance the light energy received
by the photosynthetic reaction centers ( Chow, 1994 ) .
However, under these conditions plants also produce
reactive oxygen species, which cause enhancement of
the peroxidation of membrane lipids and even destruc-
tion of the photosynthetic apparatus ( Parkin et al. ,
1989; Foyer et al. , 1994) .
The accumulation of osmolyte compounds ( e .
g ., total solublesugar andproline) in thecells is like-
ly a response to water deficit induced by chilling stress
( Gzik, 1996; Bajji et al. , 2001 ) . Osmotic adjustment
causes decrease in osmotic potential of the plant tissue
hence allows the leaves towithstand a low water poten-
tial without loss of turgor (Holbrook and Putz, 1996) .
The combined effects of low temperature and high irra-
diance are more harmful than the individual effect of
each stress on the plant (Long et al. , 1994) .
The main objective of this study was to compare
the effect of chillingnight temperatureon the photosyn-
thesis of the most two common mango cultivars in the
study region, i . e .,‘Choke Anand’and‘Khieo Sa-
woei’, and to identifywhich cultivar is more tolerant to
thepotential extreme chillingtemperatureof the region .
844 云 南 植 物 研 究 30 卷
In addition, the present study tested whether partial
shading could alleviate the adverse effect of chill-night
on photosynthesis in mango seedlings .
Materials and Methods
Study site and treatments
This study was conducted at the Xishuangbanna Tropical
Botanical Garden ( 21°56′N, 101°15′E ; 600 m altitude) , situ-
ated in the southern part of Yunnan Province, southwestern Chi-
na , the northern border of the tropics . Here the mean annual
temperature is21 .7℃ ; themeanmonthly temperature is 25 .3℃
in the hottest month ( July) and 15 .6℃ in the coolest month
(January; Liu and Li , 1996) . The mean annual precipitation is
about 1 560 mm, 80% of which falls fromMay to October .
In November 2004 , about one meter high of seedlings (two
years old) of two cultivars of mango ( Mangifera indica L .)
‘Choke Anand’and‘Khieo Sawoei’were obtained from a local
commercial nursery . The seedlings were transplanted into 15 L
pots, one seedling per pot . They were grown under two irradi-
ance levels: the full light and 50% daylight that were obtained
by using black neutral density shade nets suspended above the
plant . Theywereregularly pruned to maintain about 1 mtall pla-
ntswith single apical shoot, and were irrigated and fertilized ac-
cording to standard commercial practices . The mean daily maxi-
mum, minimum, and average temperatures during the three
weeks prior the measurements were 27.2℃ , 13 .5℃ , and
17 .13℃ . The air temperatures ( maximum, average, and mini-
mum) during the experiment were recorded by a weather station
that was situated 30 m away from the experimental plot, while
photosynthetically active radiation ( PAR ) on leaves was mea-
suredwith the thermocouple attached to the leaf clip during the
chlorophyll fluorescencemeasurement (Fig . 1) .
Fig . 1 Maximum ( max . Ta) , minimum ( min . Ta) and average air
temperatures ( ava . Ta) and photosynthetically active radiation
( PAR) at plant leaf level in both light levels (50 % and
100 % sunlight) during the experiment period
In the beginningof February 2006 , four to five potted seed-
lings of each irradiance regime per cultivar were moved into a
dark cold storage room at 4℃ from 17 .30 h to 05.30 h ( solar
time) next morning for 7 constitutive nights . They were returned
to theoriginal site for the rest of the day .
Gas exchange and chlorophyll fluorescence measurements
Using a photosynthetic system ( LI 6400 LI-COR , Inc .,
Lincoln, NE , USA ) , gas exchange of these chilling-treated
seedlings weremeasured fromtheir recent mature leaves of 4 - 5
replicate plants duringthe period from09 .00 h to12 .00 h in the
morning, under photosynthetic flux density ( PPFD) of 1 000
μmol m- 2 s- 1 that was provided by an integrated LED light
source ( LI-6400; -02B LI-COR , Inc . , Lincoln, NE , USA ) .
Theair humidity in the leaf chamber was about 60% , with CO2
concentration of 350 - 360μmol mol - 1 , with ambient air temper-
ature of 21℃- 24℃ , and flow rate of theair was 500μmol s- 1 .
Themeasurements were done on the day before chilling, on each
of 7 d duringthechill-night treatment, and subsequent four days
(1 , 3 , 7 , and 10 day) after termination of the chilling treat-
ment .
At predawn and midday of these days, chlorophyll fluores-
cencewas measured to quantify chilling injury to photosystem II
(PSII) , using afluorometer (FMS2; Hansatech, Norfolk, UK ) .
Initial ( F0 ) and maximal fluorescence ( Fm ) were measured in
the leaves that have been dark-adapted for at least 20 min . Fm
was estimated by illuminating the dark-adapted leaves with a
pulse of PPFD 5 000 mol m- 2 s- 1 for 0 .7s . Themaximum quan-
tumyield of PSII was estimated by the ratio Fv?Fm = ( Fm -
F0 )?Fm accordingto Genty et al. ( 1989 ) . Steady-state chlo-
rophyll fluorescence ( Fs ) andmaximal fluorescence in the light-
adapted state ( Fm′) were determined at incident sunlight, which
wasmeasured with a quantum sensor attached to the leaf clip .
Actual PSII quantum yield was calculated (Genty et al. , 1989)
asΦPSII = (Fm′- Fs )?Fm′.
Non-photochemical quenching, representing the absorbed
light energy dissipated as heat was calculated as ( Bilger and
Bj?rkman, 1990) : NPQ = ( Fom - Fm′)? Fm′. Predawnmax-
imal fluorescence ( Fom) was used to calculate NPQ . On the day
before, the seventh day with and the seventh day after the chill-
night treatment, the midday allocations of photons absorbed by
PSII reaction centers to photosynthetic electron transport and to
thermal dissipationwereassessedaccordingto Hendrickson et al.
(2004) . Thefraction of photons allocated to PSII photochemistry
(ФPSII ) was the same asΦPSII indicated above . The sum of the
fractions of the light that was lost by either constitutive thermal
dissipation (ФD ) or viafluorescence (Фf ) was derived asФf ,D =
Fs?Fm , and thefractionof light thatwas dissipatedviaΔpH and
9444 期 Nabil I . Elsheery et al . : The Effect of Night Chilling on Gas Exchange and Chlorophyll Fluorescence . . .
xanthophyll-regulated process wasФNPQ = Fs?Fm′- Fs?Fm .
Determination of chlorophyll , MDA content and membrane
leakage
On the daybefore, the seventh dayof night chillingand the
seventh day after chilling-treatment, leaves similar to those used
for physiological measurements were sampled to determine their
chlorophyll and carotenoid contents following Lichtenthaler and
Wellburn ( 1983) , and malondialdehyde (MDA) content accord-
ing to Hodges et al. (1999) , using a spectrophotometer ( UV-
B2501 ; Shimadzu; Kyoto, Japan) . MDA is a product of peroxi-
dation of membrane lipids .
Some leaves were used to measure membrane leakage .
Leaf′s discs were rinsed three times in ion-free water, dried on
degreased-gauze, and ten discs were transferred into each test
tube . Ion-free water (20 ml ) was added into each of the test tubes
and thetest tubes were vacuum- infiltrated and shaken for 1 h in a
shaker (WD . 940.5B . Beijing 61, Beijing, China) at the room
temperature . The conductance (R1) of the liquid in each test tube
was measured with an electrode conductivity meter (DOS-307 , Lei-
ci, Shanghai , China) . Afterwards, the tubes were capped, boiled
for 30 min, and then cooledto roomtemperatureand shakenfor 1 h
at the room temperature . The conductance ( R2) of the liquid in
each test tubewas measuredonceagain . The ratioof thetworead-
ings ( R1?R2) was used as a measure of the relative injury .
Determination of contents of proline and total soluble sugars
Using the leaf samples collectedon thethreedays indicated
above, extraction and estimation of free proline were conducted
according to the procedures described by Bates et al. ( 1973 ) .
The dry leaf sample of 500 mg for each cultivar was homogenized
in 10 cm3 of 3% (m?v) aqueoussulphosalicylic acid and theho-
mogenatewas filtered through Whatman No . 2 filter paper . In a
test tube, 2 cm3 of the filtrate was mixed with 2 cm3 acid nin-
hydrin and 2 cm3 glacial acetic acid and incubated in 100℃ wa-
ter bath for 1 h . The reaction was terminated by placingthetube
in ice bath and then extracted with 4 cm3 toluene . The chro-
mophorephase was aspirated fromtheaqueous phase . The absor-
bance was read at 520 nmusing thesame spectrophotometer . Ac-
cordingtoDubois et al. (1956) , thecontent of total soluble sugar
was estimated using the phenol sulphuric acid .
Statistical analysis
The difference in the means of chlorophyll and MDA cont-
ent, membrane leakage, and contents of proline and total soluble
sugars among different days for the same cultivar under the same
irradiance were analyzed withone-wayANOVA . Differenceswere
considered significant at a probability level of P≤ 0.05 . Two-
way ANOVA was used to evaluate effects of cultivar, irradiance
and their interaction on the physiological traits .
Results
Gas exchange and chlorophyll fluorescence
The exposure to4℃ for seven consecutive chilling
nights led to a progressive decline innet photosynthesis
( Pn ) and stomatal conductance ( gs ) in both mango
cultivars ( Fig . 2 ) under both irradiances, with the
sharp decreases following the first chillingnight . These
decreases weremore pronounced in the seedlings under
full light than thoseunder 50% sunlight . In both culti-
vars, Pn increased linearly from the first day to the
seventh day after the chilling treatment, with almost
complete recovery on the seventh day .
Maximum photochemical efficiency ( Fv?Fm ) at
predawn and midday, and actual photochemical effi-
ciency of PSII (ΦPSII ) followed the similar changing
trend of Pn in both mango cultivars ( Fig . 3) . During
the chill-night treatment, both predawn and midday
value of Fv?Fm andΦPSII kept declining with increas-
ing in thenumber of chillingnightsbut thisdeclinewas
stronger and attained lower value for‘Khieo Sawoei’
cultivar than‘Choke Anand’cultivar under the same
irradiances (Fig . 3 ) . The recovery of Fv?Fm values at
predawn and midday in both cultivars were almost com-
pleted after seven days since termination of the chilling
treatment .
NPQ rates increased with the number of chilling
nights for both cultivars but this increase was stronger
and attained greater value for‘Choke Anand’compare
to‘Khieo Sawoei’cultivar for both irradiances . The
NPQ rates decreased following the termination of the
chilling treatment (Fig . 3) .
On the day before treatment, after 7 day of chill-
ing treatment and after 7 day of recovery, thefateof ab-
sorbed light energy in the leavesof bothmango cultivars
was evaluated (Fig . 4 ) .The results showed thatΦNPQ
was significantly higher while ΦPSI I was significantly
lower after 7 nights of chilling treatment under both
light regimes . Meanwhile the decrease of Φf , D was not
pronounced under both light regimes . After 7 nights of
chilling treatment, about75% and 55% of the absorbed
light were dissipated thermally for the seedlings under
full light and 50% daylight, respectively (Fig . 4) .
054 云 南 植 物 研 究 30 卷
Fig . 2 Net photosynthetic rates ( Pn) and stomatal conductance ( gs ) in two mango cultivars grown under two irradiances, measured in the
morning on the day before treatment (cont) , seven days with the chill-night treatment (1 - 7) , and 10 days after termination the treatment ( 1a
- 10a) . Symbols and bars denote means±SE (n = 5)
Contents of photosynthetic pigments and MDA
The chlorophyll ( Chl ) content was lower, while
carotenoid?chlorophyll ratio ( Car?Chl ) tended to be
higher with increase in the growth irradiance in both
cultivars after the chill-night treatment . The‘Choke
Anand’ cultivar had higher Chl contents and lower
MDA contents and membrane leakage ( EC% ) values
than‘KhieoSawoei’cultivar after the chill-night treat-
ment . Thedecrease in Chl content and increase in Car?
Chl , EC% and MDA were greater in seedlings under
the full irradiance than 50% daylight for both culti-
vars . During the chilling treatment, some chlorosis of
leaf blades was observed in sun-exposed seedlings in
both cultivars, whileno chlorosis foundon theleavesof
the seedlings under 50% daylight .
Contents of proline and total soluble sugars
The chilling treatment resulted in an increase in
the contents of proline and total soluble sugars under
both irradiance regimes ( Table 1 ) , with greater in-
crease for seedlings in full irradiance than in 50% day-
light . The‘Choke Anand’cultivar had higher contents
of soluble sugar and proline compared to‘Khieo Sa-
woei’cultivar after the chilling treatment .
The two-way ANOVA results reveal significant
differences between the two cultivars inΦPSII , dawn
Fv?Fm , NPQ, and contents of MDA , Proline and TSS
but no significant difference between cultivars in Pn ,
gs , midday Fv?Fm , Chl a + b, Car?Chl and EC%
(Table 2 ) . Moreover, all the physiological parameters
were significant different between the light levels . The
effects of light level on physiological parameters were
more pronounced than the cultivar . The effect of inter-
action between light and cultivar wasonly significanton
Pn and gs .
1544 期 Nabil I . Elsheery et al . : The Effect of Night Chilling on Gas Exchange and Chlorophyll Fluorescence . . .
Fig . 3 Maximum photochemical efficiency ( Fv?Fm) of photosystemII at predawn andmidday, andmidday actual quantum yield of photosystem
II (ΦPSII ) and non-photochemical quenching ( NPQ) in two mango cultivars grown under two irradiances, on the day before treatment (cont) ,
seventh days with ( 1 - 7) , and 10 days after termination the chilling treatment (1a- 10a) . Symbols and bars denote means±SE (n= 5)
Discussion
The present study showed that the chill-night
treatment induced strong depression of Pn during the
subsequent days for both studied cultivars ( Fig . 2 ) .
This is consistent with theprevious studieson thetropi-
cal plants (Nir et al. , 1997; Allen et al. , 2000; Guo
and Cao, 2004; Feng and Cao, 2005) . However, the
effects of chilling treatment on the present mango seed-
lings were less pronounced compared to the coffeespecies
(Guo andCao, 2004) and the tropical trees Calophyllum
254 云 南 植 物 研 究 30 卷
Fig . 4 Thepartitioning of absorbed light energy on midday in twomango cultivars grown under two irradiances, on theday before treatment (Be-
fore T ) , the seventh day with (After T ) and the seventh day after the chilling treatment ( After R) . Symbols and bars denotemeans±SE ( n= 5)
Table 1 Chlorophyll (Chl a+ b) content, carotenoid: chlorophyll ratios ( Car?Chl) , membrane leakage (EC% ) , malondialdehyde ( MDA )
content, proline content and total soluble sugar content (TSS) in two mango cultivars (‘Choke Anand’and‘Khieo Sawoei’) on the
day before treatment ( A ) , the seventh day (B) since chill-night treatment and the seventh day since the termination of the
chilling treatment (C) . Both cultivars were grown under 100 % and 50 % sunlight . Different letters within the same
parameters under the same irradiances indicate significant differences in the means of the same cultivars ( P < 0 .05) .
Light
intensity
Chl a+ b
( mg g - 1 ?FW) Car?Chl EC%
MDA
( nmols g - 1 FW)
Proline
(μmol g- 1 pDW)
TSS
( mg g - 1 DW )
‘Choke Anand’
A 2 ?. 32±0 .11a 0 . 252±0 . 016a 9 }. 3±1 >. 3a 14 . 1±1 .1a 2 .6±0 ^. 3a 46 @. 4±4 ?. 1a
100 ?% B 1 . 57±0 . 13b 0 .373±0 .013b 28 .9±1 O. 1b 51 ?. 3±1 .7b 5 . 8±0 \. 2b 85 >. 7±3 .6b
C 2 ?. 21±0 .08a 0 . 262±0 . 018a 11 .6±1 Q. 7a 17 . 2±1 .0a 3 .2±0 ^. 2a 53 @. 3±4 ?. 8a
A 2 ?. 97±0 .11a 0 . 221±0 . 022a 7 }. 1±1 >. 4a 9 ?. 1±0 . 9a 2 .0±0 ^. 1a 39 @. 3±2 .7a
50 ?% B 2 . 33±0 . 17b 0 .272±0 .017b 21 .3±1 O. 1b 35 ?. 7±1 .7b 3 . 9±0 \. 3b 68 >. 2±3 .8b
C 2 ?. 82±0 .074a 0 |. 231±0 .016ab 8 }. 9±1 >. 3a 11 . 7±0 .9a 2 .1±0 ^. 1a 43 @. 7±4 ?. 0a
‘Khieo Sawoei’
A 2 ?. 24±0 .15a 0 . 231±0 . 018a 10 .1±1 Q. 3a 15 . 7±1 .5a 2 .3±0 ^. 2a 43 @. 2±4 ?. 7a
100 ?% B 1 . 51±0 . 08b 0 .347±0 .016b 32 .9±1 O. 0b 64 ?. 3±1 .8b 5 . 5±0 \. 1b 82 >. 2±3 .1b
C 2 ?. 05±0 .10a 0 . 257±0 . 014a 10 .8±1 Q. 1a 19 . 5±2 .3c 2 .9±0 ^. 1a 46 @. 7±2 ?. 4a
A 2 ?. 77±0 .11a 0 . 208±0 . 017a 8 }. 0±1 >. 8a 10 . 6±0 .8a 1 .6±0 ^. 2a 37 @. 3±3 ?. 9a
50 ?% B 2 . 19±0 . 08b 0 .261±0 .014b 23 .6±1 O. 6b 43 ?. 2±1 .5b 3 . 2±0 \. 1b 50 >. 9±3 .0b
C 2 ?. 72±0 .17a 0 |. 211±0 .013ab 9 }. 3±1 >. 4a 12 . 9±1 .0c 1 .9±0 ^. 1a 39 @. 1±2 ?. 8a
3544 期 Nabil I . Elsheery et al . : The Effect of Night Chilling on Gas Exchange and Chlorophyll Fluorescence . . .
Table 2 The two-way ANOVA result on the effect of cultivar and irradiance on various physiological parameters
Parameter
Cultivar
F P
Light intensity
F P
Interaction
F P
Pn 0 ?. 090766 ns 48 X. 781 * 19 S. 46616 *
gs 0 ?. 041426 ns 24 3. 62407 * 13 S. 89751 *
Dawn Fv?Fm 5 ?. 021605 * 24 3. 10188 * 0 .. 210357 ns
Midday Fv?Fm 2 ?. 595906 ns 66 3. 23515 * 1 .. 654176 ns
ФPSII 10 ?. 12924 * 440 X. 5738 * 1 .. 070911 ns
NPQ 4 ?. 937512 * 17 3. 99851 * 0 .. 001571 ns
Chl a+ b 1 .06994 ns 53 3. 17999 * 0 .. 135114 ns
Car?Chl 1 ?. 583122 ns 37 3. 97655 * 0 .. 167574 ns
EC% 4 ?. 322181 ns 29 3. 55097 * 0 .. 299146 ns
MDA 66 ?. 22471 * 218 X. 1706 * 3 .. 841054 ns
Proline 10 %. 7084 * 174 X. 9523 * 1 .. 181721 ns
TSS 8 ?. 777987 * 107 j. 416 * 1 .. 312286 ns
ns, insignificant difference at P > 0 . 05; * significant difference at P < 0 . 05 .
polyanthum and Linociera insignis ( Feng and Cao,
2005) in thesame study areawith the same night-tem-
perature treatment reported in previous studies .
The parallel reduction in both gs and Pn during
the chilling treatment suggests the involvement of sto-
matal limitation to photosynthesis, as found as a posi-
tive response tochilling in numerous species, including
mango ( Nir et al. , 1997; Allen et al. , 2000 ) , olive
( Bongi and Long, 1987 ) , grapevine ( Flexas et al. ,
1999) and coffee species (Guo and Cao, 2004) . Chill
nights can cause increase in resistance to water absorp-
tion fromthesoil anddecrease in hydraulic conductivity
of xylem (McWilliam et al. , 1982; Pavel and Ferees,
1998) . Consequently, the plantsmay suffer fromsome
degree of water deficit, resulting in the reduction of
stomatal conductance . A decrease of stomatal conduc-
tance under these conditions is helpful for the plants to
prevent excessive water loss .
Decreases in Fv?Fm and ΦPSII , along with in-
crease in NPQ or ΦNPQ , were similar in both mango
cultivars following the chilling treatment ( Fig . 3 and
4) . Overall , the results indicated that the chill-night
treatment induced suppression in the photosynthesis of
themango leaves up to chronic photoinhibition in case
in the seedlings under full light, as also reported by
previous studies onmango after chill night (Nir et al. ,
1997; Allen et al. , 2000 ) . This is also in agreement
with other studies on other tropical plants in the same
study area ( Guo and Cao, 2004; Feng and Cao,
2005) . High fraction of absorbed energy dissipated as
heat under low temperature as indicated by increasing
ΦNPQ is helpful to minimize the damaging potential of
excess energy especially in fully open site (Sveshnikov
et al. , 2006; Hendrickson et al. , 2004) . The greater
NPQ in‘Choke Anand’ ( Fig . 3 ) explain a higher
light energy dissipation, which must result in a less ex-
cessive energy load on the photosynthetic apparatus
than in‘Khieo Sawoei’. Our previous study (Elsheery
et al. , 2007) has alsoshown that‘ChokeAnand’cul-
tivar is chilling-tolerant compared to other cultivars
grown in a common garden in the same site as the pr-
esent study . The fast recovery of chlorophyll fluores-
cenceparameters in both mango cultivars suggests that
the decline in PSII efficiencywas reversible, serving as
a photoprotective role against chilling stress under both
irradiances . Moreover, every day during the winter
season in Xishuangbanna, thereis heavyfog cover from
midnight until noontime of the following day (Liu and
Li , 1996) . The fog blocks direct sun, thereby reduc-
ing the adverse effects of chilly night temperatures on
tropical plants .
Chilly night temperatures resulted in adecreaseof
chlorophyll content, while increasing of Car?Chl ratio
in both mango cultivars and two irradiances . The ex-
cessive light energy can cause the oxidation of chloro-
phyll . Carotenoids acts as photoprotective pigments by
avoiding the generation of singlet oxygen by quenching
the triplet-state chlorophyll molecules and by scaveng-
ing any singlet oxygen produced thus avoiding chloro-
phyll photoxidation (Young, 1991) . Xanthophyll is the
454 云 南 植 物 研 究 30 卷
main carotenoid component that is involved in light en-
ergy dissipation (Demmig-Adams and Adams, 1992 ) .
Thus, the large increase in NPQ, and the ratio of total
carotenoids to Chl a+ b, in both mango cultivars after
chilling nights ( Fig . 3 , Table 1 ) , can be considered
as positive response to dissipate the excessive light en-
ergy in mango cultivars .
Excess light energy can also enhanceproductionof
free oxygen radicals, which lead to peroxidation of fatty
acids in cell membranes ( Parkin et al. , 1989; Foyer
et al. , 1994) . In thepresent study, higher concentra-
tion of MDA , which is the product of lipid peroxida-
tion, in the leaves of the mango cultivars after chilling
treatment (Table 1 ) , indicated an increased oxidative
stress in these leaves .
The accumulation of osmolyte compounds in the
cells is likely a response to water deficit induced by
chilling stress, which seems to act as a survival mecha-
nismfor the plant under stress ( Gzik, 1996; Bajji et
al. , 2001) . Osmotic adjustment causes decrease in the
osmotic potential of the plant tissue hence allow the
leaves to withstand a lower water potential without loss
of turgor (Holbrook and Putz, 1996) . Accumulationof
compatible solutes is cryptoprotective mechanism in
some plants ( Alberdi and Corcuera, 1991 ) . Proline
accumulates in many plants species under stress condi-
tions to protect foldedprotein structure against denatur-
ation, stabilizes cell membrane by increasing interact-
ing with phospholipids, functions as hydroxyl radical
scavenger, or serves as an energy and nitrogen source
(Aspinall and Paleg, 1981; Samaras et al. , 1995 ) .
In conclusion, the night chilling resulted in a se-
vere reduction of gas exchange rates and photochemical
efficiency in both mango cultivars . The reduction in
these parameters was stronger in the mango seedlings
grown under full light than in those under 50% day-
light . Chill-night treatment induced photoinhibition in
seedlings in full light, which was recovered after a
week after the chilling treatment .Thequick recovery in
gas exchange parameters and chlorophyll fluorescence
indicate that both mango cultivars are actually quite
chilling tolerant but the‘ Choke Anand’ cultivar
showed higher resistance to chilling than‘Khieo Sa-
woei’cultivar as indicated by theslower recovery of the
latter . Shading significantly mitigated adverse effect of
chilling nights .
Acknowledgements: The Graduate University of the Chinese
Academy of Sciences provided a fellowship to N . I . E . The au-
thors thank Wei Yan for selection and providing information on
themango cultivars and Yan-juan Jiang for technical assistance
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