全 文 ：高山植物圆锥南芥的光合系统耐热性及其修复机制
*
唐 婷1，2，郑国伟1，李唯奇1＊＊
(1 中国科学院昆明植物研究所中国西南野生生物种质资源库，昆明 650201;2 中国科学院大学，北京 100049)
摘要:高温胁迫包括极端高温和中高温，严重影响了植物的一系列生理活动，尤其是光合作用，而植物应
对极端高温和中高温胁迫具有不同的策略。高山植物因长期生长于相对寒冷的环境中，相比而言应缺少对
高温胁迫的适应机制。本文以圆锥南芥作为一种高山模式植物来探索其在中高温下是否表现出耐热能力，
如果具有耐热能力，那么在光合方面与拟南芥存在怎样的差异。研究发现，圆锥南芥在中高温处理后具有
更高的光化学效率及快速可逆的恢复过程，表现出了较强的耐热能力。两物种的 F0没有明显的差异，而
圆锥南芥在热处理后及恢复过程中具有更高的 Fm，促进其快速光合修复。在热处理后，非光化学能量耗
散快速瞬时上升，及时保护光系统 II免受光损伤和热伤害，另外，HSP101 蛋白迅速诱导可能启动了光化
学修复。最后，圆锥南芥在严重高温处理后具有更高的存活率再次验证了它在中高温下的耐热能力。结果
表明，圆锥南芥具有更耐热的光合系统以及有效的光合修复机制来耐受中高温胁迫。
关键词:高温胁迫;中高温胁迫;光合作用;圆锥南芥;非光化学能量耗散;热激蛋白
中图分类号:Q 945 文献标志码:A 文章编号:2095－0845(2015)01－046－09
The Thermotolerance and Ｒepair Mechanism of Photosystem
in Alpine Plant Arabis paniculata (Cruciferae)*
TANG Ting1，2，ZHENG Guo-wei1，LI Wei-qi1＊＊
(1 Germplasm Bank of Wild Species in Southwest China，Kunming Institute of Botany，Chinese Academy of Sciences，
Kunming 650201，China;2 University of Chinese Academy of Sciences，Beijing 100049，China)
Abstract:The heat stress associated with extremely and moderately high temperatures affects a series of physiologi-
cal activities in plants especially photosynthesis． However，it is proposed that the plants use different photosynthetic
strategy to deal with extreme and moderate heat stresses． Most reports focus on the cold tolerant ability but thermotol-
erance of alpine plants． In the present study，we used the alpine plant Arabis paniculata as a model alpine plant to
examine whether its capacity for heat tolerance is exhibited under moderate heat stress and，if so，how this capacity
is related to differences in its photosynthesis compared with that of its close relative Arabidopsis thaliana． We found
that A. paniculata had high photochemical efficiency at a moderately high temperature and a rapid reversible recovery
process，which reflected substantial heat tolerance． Despite no obvious difference in F0 between the two species，the
higher Fm values after heat treatment and recovery in A. paniculata than in A. thaliana facilitated the rapid photo-
chemical recovery． A rapid and transient increase in non-photochemical quenching after moderate heat stress provid-
ed timely protection for PSII against the damage caused by heat and light． The rapid accumulation of heat shock pro-
tein 101 upon exposure to moderately high temperatures might initiate photochemical repair． Finally，the high rate of
survival of A. paniculata after severe heat treatment attested to the substantial heat tolerance of its photosynthetic ma-
chinery under moderate stress． Our results indicated that a highly heat-tolerant photosystem and effective photochemi-
植 物 分 类 与 资 源 学 报 2015，37 (1):46～54
Plant Diversity and Ｒesources DOI:10．7677 /ynzwyj201514037
＊
＊＊
Funding:NSFC (31300251)and XiBuZhiGuang Project
Author for correspondence;E-mail:weiqili@mail. kib. ac. cn
Ｒeceived date:2014－03－12，Accepted date:2014－06－11
作者简介:唐婷 (1987－)女，博士，主要从事植物逆境分子生理学研究。E-mail:tangtingnkjdx@163. com
cal repair mechanism contribute to the capacity of A. paniculata to tolerate moderate heat stress．
Key words:Heat stress;Moderate heat stress;Photosynthesis;Arabis paniculata;Non-photochemical quenching;
Heat shock protein
Heat stress caused by the exposure of plants to
temperatures beyond their optimum is a major factor
that limits crop production worldwide (Hall，2010)．
High temperature can affect many physiological ac-
tivities throughout the life cycles of plants． Photosyn-
thesis is one of the most heat-sensitive process in
plants and is often completely inhibited before the
symptoms of other injuries appear． Heat stress can
be classified into moderate and extreme according to
duration of stress，time of the day at which it occurs
and co-exposure to other stresses，each of which in-
volves different coping mechanisms and adaptation
strategies (Berry and Bjorkman，1980;Blum，1988)．
Such temperature stress occurs regularly in alpine
environments (Krner，2003)． An extremely high
temperature could cause severe cellular injuries and
even a catastrophic collapse of cellular organisation
within minutes (Schffl et al．，1999)． However，
significant and rapid reversible changes in photosyn-
thetic metabolism caused by moderately high leaf
temperature might differ from irreversible damage
brought about by severe heat stress． These changes
under moderate heat stress can help us understand
how heat is tolerated by photosynthetic systems and
provide insight into how plants could be made more
heat-tolerant through genetic modification (Sharkey
and Zhang，2010)．
Photosystem II (PSII)，as a protein complex
involved in photosynthesis is shown to be partially
inhibited by a moderately high temperature (Song et
al．，2010)． Chlorophyll fluorescence is a sensitive
and reliable indicator of the changes caused by heat
stress in components of the photosynthetic appara-
tus，such as PSII (Krause and Weis，1991;Govin-
dje，1995;Strasser，1997)． The ratio of variable
fluorescence to maximum fluorescence (Fv /Fm)，
the minimal fluorescence (F0)，and the maximal
fluorescence (Fm)are important physiological pa-
rameters that are closely related to thermotolerance
(Yamada et al．，1996)． For example， in bean
plants，the initial F0 level clearly increases after
heat treatment and then declines 4 h after recovery
(Petkova et al．，2007)． In oak leaves，PSII could
be protected from heat-dependent photo-inhibition
via NPQ，which dissipates excess excitation energy
(Haldimann and Feller，2004)． Allakhverdiev et al．
(2008)also found that exposure to a moderately
high temperature did not result in severe damage to
PSII，but it did inhibit its repair． Most reported
studies concentrated on the process immediately after
heat shock，but there is little information about the
PSII changes during the post-heat stress recovery
process． However，the recovery from heat stress is
very significant for plants to survive in complex and
variable environments． Thermal inactivation of PSII
is slowly reversible and the recovery process is
known to take several days (Seemann et al．，1984;
Bilger et al．，1987;Karim et al．，1999)． It is vital-
ly important to study the exact photosynthetic re-
sponse over the period from heat treatment to the re-
covery process lasting several days．
The photochemical response to moderate heat
stress and during the subsequent recovery process
might be closely associated with certain biochemical
activities． For instance，heat shock proteins (HSPs)
may help in the degradation of proteins damaged by
heat stress (Parsell and Lindquist，1993)． Chloro-
plast HSPs play a role in the prevention of stress-re-
lated damage rather than in the repair of such dam-
age (Downs et al．，1999)． However，whether HSP101
functions in the process of photochemical repair has
not been described．
Arabis paniculata，a relative of Arabidopsis thali-
ana，lives in alpine environments that experience
moderately high temperatures (about 30 ℃)in some
seasons (Zheng et al．，2011)． Against the above
741期 TANG Ting et al．:The Thermotolerance and Ｒepair Mechanism of Photosystem in Alpine Plant …
background，the current study is intended to answer
the following questions:Can A. paniculata tolerate
exposure moderate increases in temperature?If so，
how does its photosynthetic machinery respond?In
addition，are these traits consistent with its thermo-
tolerance under an extremely high temperature?As
such，the specific aim of this study was to use chlo-
rophyll fluorescence to compare the heat tolerance of
PSII in A. paniculata with that of A. thaliana after
moderate heat treatment and during the subsequent
recovery stage lasting several days． We next meas-
ured a biochemical factor that might affect the photo-
chemical repair process，namely，the accumulation
of HSP proteins，in both species after heat shock
and during recovery． Finally，we verified the heat
tolerance of A. paniculata under a moderately high
temperature comparing the survival rates of these two
species under severe heat stress．
1 Methods and materials
1. 1 Plant material
Arabis alpina，which is synonymous with A. panic-
ulata，distributed widely in most mountain systems
in European，East Africa，Central Asia and so on
(Koch et al．，2006)． Seeds of A. paniculata were
collected from Lijiang mountain (North latitude
26. 86 and East longitude 100. 25)with a altitude of
more than 2 500 m in Yunnan Province． A. thaliana
is mainly originated from Europe，Asia，and north-
western Africa (http:/ / en. wikipedia. org /wiki /Ar-
abidopsis thaliana)． All known ecotypes of Arabidop-
sis are not tolerant to abiotic stresses (Bressan et
al．，2001)． All studies involved seedlings (9 days
after germination with 2 leaves)and mature plants
(4 weeks grown in soil with a rosette of more than 6
leaves)of A. paniculata and A. thaliana (Columbia
ecotype)． The HSP101-depleted mutant hot-1 (Salk
066374)of Arabidopsis (Columbia ecotype)was de-
scribed previously (Zhang et al．，2010)．
1. 2 Plant growth and heat treatments
Seeds of A. paniculata and A. thaliana were ster-
ilised with ethanol (75%)for 2 min and sodium hy-
pochlorite (5%)for 2 min，followed by three wa-
shes with sterile distilled water． After surface steril-
isation，the seeds were cold-stratified for four days at
4 ℃ and sown on Murashige and Skoog (MS)medi-
um containing 1% sucrose． The seeds were germina-
ted and grown at 22 ℃ with a 12 h light /12 h dark
photoperiod with a photosynthetic photon flux density
of 120 μmol·m－2·s－1 for 9 days． Plates with seedlings
were treated at 37 ℃ for 2 h (72 μmol·m－2·s－1)
and then left at 22 ℃ (4 μmol·m－2·s－1)for 1 h，
before 1 h of heat treatment at 48 ℃ in the dark，
and then left at 22 ℃ (4 μmol·m－2·s－1)for 3 days
of recovery． For the soil-grown plants，4-week-old
seedlings were exposed to 45 ℃ for 2 h in the dark
and then left at 22 ℃ (4 μmol·m－2·s－1)for 3 days
of recovery． For the survival rate test，9-day-old
plated seedlings were treated at 45 ℃ for 3 h in the
dark and then left at 22 ℃ (4 μmol·m－2·s－1)for
recovery．
1. 3 Measurement of chlorophyll fluorescence
Chlorophyll fluorescence was measured using an
IMAGING-PAM chlorophyll fluorometer and the Im-
aging Win software application (Walz，Effeltrich，
Germany)，as described previously (Woo et al．，
2008)． A dark-light induction curve was applied to
assess dark- and light-adapted parameters． Plants
were given a saturating pulse (＞1 800 μmol photons
·m－2·s－1)and the levels of F0，Fm，and Fv /Fm
were determined after 20 min of dark adaptation． Fv /
Fm was calculated as (Fm － F0)/Fm ． False-colour
images of the Fv /Fm parameter are presented through
the Imaging Win software (Woo et al．，2008)． After
40 sec of exposure in the dark and a subsequent 6
min of actinic illumination (111 μmol photons·m－2
·s－1)with saturating flashes at intervals of 20 sec-
onds，the actual quantum yield of PSII photochemis-
try［Y(II)］，the yield of regulated energy dissipa-
tion［Y(NPQ) ］，the yield of non-regulated energy
dissipation［Y(NO) ］，and an estimate of the frac-
tion of open PS II centres (qL)were obtained after
another 6 min of light adaptation before taking the fi-
nal measurements．
84 植 物 分 类 与 资 源 学 报 第 37卷
1. 4 Protein extraction and immunoblotting of
HSPs
Total protein was isolated according to a previ-
ously described procedure (Fan et al．，1997)．
Seedlings were ground with homogenisation buffer
(50 mmol·L－1 Tris-HCl，pH 7. 5;10 mmol·L－1
KCl，1 mmol·L－1 ethylenediaminetetraacetic acid，
0. 5 mmol·L－1 phenylmethylsulfonyl fluoride and 2
mmol·L－1 dithiothreitol)in a precooled mortar． Af-
ter centrifugation at 7 000 r·min－1 for 10 min at 4 ℃，
the amount of protein in the supernatant was deter-
mined at 595 nm using a dye-binding assay with
Coomassie Brilliant Blue． The same amount of total
protein was separated by sodium dodecyl sulfate
polyacrylamide gel electropheresis analysis and then
transferred onto polyvinylidene difluoride filters．
These filters were first probed with HSP101-specific
antibodies，and then incubated with a secondary an-
tibody conjugated to alkaline phosphatase． HSPs
were visualised by staining the blot for phosphatase
activity． Each measurement was performed independ-
ently at least three times．
2 Ｒesults and discussion
2. 1 A. paniculata exhibited superior photochem-
ical efficiency after moderate heat treatment and
more rapid recovery than A. thaliana
We detected the maximal photochemical effi-
ciency in A. paniculata and A. thaliana under moder-
ate heat shock and during the subsequent recovery
period in order to compare the heat tolerance of PSII
between these species． As shown in Fig. 1，Fv /Fm
declined after all three heat treatments and increased
reversibly after several days of recovery in both
plants． This suggested that these three types of heat
treatment constituted moderate stress for the plants．
After 40 min at 48 ℃ with heat acclimation，Fv /Fm
remained at about 0. 4 in A. paniculata，but it de-
clined to almost 0 in A. thaliana (Fig. 1A)． With in-
creasing time at high temperature，Fv /Fm declined
to 0 after heat treatment but began to increase during
the recovery stage in both plants． The speed of this
increase was more rapid in A. paniculata than in
A. thaliana． These results suggest the substantial
thermotolerance of PSII during the early development
of A. paniculata seedlings under moderate heat
stress． To assess the thermotolerance of PSII of
A. paniculata in mature plants we measured the Fv /
Fm of 4-week-old soil-grown seedlings in A. paniculata
and A. thaliana under a moderately high temperature
(Fig. 1B)． Fv /Fm declined slightly in A. paniculata
and more substantially in A. thaliana after 2 h at
45 ℃，and it recovered to the normal state more rap-
idly in A. paniculata than in A. thaliana． All of these
findings indicated the considerable heat tolerance of
the photosynthetic machinery of A. paniculata at all
development stages． This tolerance might help A. pan-
iculata to adapt to the daily increases in temperature to
the moderate levels that occur in alpine environments．
2. 2 The heat response pattern of F0 and Fm pro-
vided the basis for the rapid recovery of Fv /Fm
in A. paniculata
In order to study the factors that affect the rapid
reversible changes in Fv /Fm of A. paniculata under
moderate heat stress，we measured F0 and Fm in this
species and in its relative A. thaliana． Both F0 and
Fm were measured after 1 h at 48 ℃ with heat accli-
mation and during the subsequent recovery stage
(Fig. 2)． After heat shock，the Fv /Fm ratio de-
creased to about 0. 2 in A. paniculata and to 0 in
A. thaliana． It then increased more rapidly in A. pan-
iculata than in A. thaliana during the recovery stage．
Meanwhile，a similar continuous increase in F0 in-
creased was observed in both plants throughout the
periods of heat shock and recovery． Whereas Fm de-
creased after heat treatment，it tended to increase
during the subsequent recovery stage in both plants．
This less marked decline and greater increase of Fm
might account for the more rapid recovery of Fv /Fm
in A. paniculata than in A. thaliana． Whereas the in-
crease in F0 indicated reduced function of the light-
harvesting complex，the decrease in Fm，which prob-
ably resulted from a change in the structure of PSII，
suggested a decrease in its photochemical efficiency
941期 TANG Ting et al．:The Thermotolerance and Ｒepair Mechanism of Photosystem in Alpine Plant …
(Mishra and Singhal，1992;Petkova et al．，2009)．
The strong thermotolerance of A. paniculata might be
closely related to the thermostability of PSII under
moderate heat treatment and the rapid reversible re-
pair of the photosynthetic apparatus．
2. 3 Non-photochemical quenching improved
the recovery of actual photochemical efficiency
by reducing photodamage in A. paniculata
Given that Fv /Fm might not comprehensively reflect
actual photochemical activities，we next investigated
Fig. 1 A． False-colour imaging of the parameter that indicates maximum quantum yield of PSII (Fv /Fm) in seedlings of
A. paniculata and A. thaliana after 1 h of exposure to 48 ℃ after heat acclimation (37 ℃ for 2 h，72 μmol·m－2·s－1)and during the
subsequent recovery period．“Ｒ 1 h”means 1 h of recovery at 22 ℃ after heat treatment，and so on;B． False-colour images of the
maximum quantum yield of PSII (Fv /Fm)of 4-week-old soil-grown seedlings of A. paniculata and A. thaliana after 2 h of heat treat-
ment at 45 ℃ and during the subsequent recovery period．“Ｒ 1 d”means 1 d of recovery at 22 ℃ after heat treatment，and so on
05 植 物 分 类 与 资 源 学 报 第 37卷
Fig. 2 The maximum quantum yield of PSII (Fv /Fm)，the minimal
fluorescence yield (F0)，and the maximal fluorescence yield (Fm)of
plated seedlings of A. paniculata and A. thaliana after 1 h of heat treat-
ment at 48 ℃ with heat acclimation (37 ℃ for 2 h，72 μmol·m－2·
s－1)and during the subsequent recovery period． Solid and dashed
lines represent A. paniculata and A. thaliana，respectively． “1 d”
means 1 d of recovery at 22 ℃ after heat treatment，and so on． An as-
terisk means that the value in A. paniculata is different from that in
A. thaliana in the same treatment (P ＜ 0. 05)
the response pattern of actual photochemical efficien-
cy Y(II)after moderate heat treatment (Fig. 3)． As
shown in Fig. 3，the overall pattern of change of Y(II)
was consistent with that of Fv /Fm after heat treatment
in both plants． Although the light energy absorbed by
the plants could be used primarily for photochemical
activities，some of it dissipated as heat by NPQ
(Hendrickson et al．，2004;Kramer et al．，2004)．
After heat treatment，Y(NPQ)increased to a peak
in A. paniculata，but it declined to 0 in A. thaliana，
and then returned to its respective control levels in
both plants． This indicated that Y(NPQ)protected
the photosystem only transiently after heat treatment
in order to improve the recovery of Y (II) in
A. paniculata． The pattern of change of qL was con-
sistent with Y(II)throughout this whole process in
both plants． There was a more marked increase in
Y(NO)in A. thaliana than in A. paniculata． An in-
crease in Y(NO)to close to 1 in A. thaliana might
indicate an almost complete breakdown in photo-
chemistry． All of these results suggest that Y(NPQ)
might protect the photosynthetic apparatus by lesse-
ning the injuries caused by heat damage and photo-
damage in A. paniculata;the reduced level of dam-
age might eventually accelerate the recovery of pho-
tochemical efficiency．
Fig. 3 The actual photochemical efficiency of PSII［Y(II)］ and the yield of regulated energy dissipation［Y(NPQ) ］，an estimate of the
fraction of open PS II centres［qL］，and the yield of non-regulated energy dissipation［Y(NO) ］in A. paniculata and A. thaliana upon 1 h
of heat treatment at 48 ℃ with heat acclimation (37 ℃ for 2 h，72 μmol·m－2·s－1)and during the subsequent recovery period． Solid and
dashed lines represent A. paniculata and A. thaliana，respectively．“1 d”means 1 d of recovery at 22 ℃ after heat treatment，and so on． An
asterisk means that the value in A. paniculata is different from that in A. thaliana in the same treatment (P ＜ 0. 05)
151期 TANG Ting et al．:The Thermotolerance and Ｒepair Mechanism of Photosystem in Alpine Plant …
2. 4 The induction of HSP101 affected the pho-
tochemical recovery process in A. paniculata
The rapid increase in HSP101 abundance after
exposure to high temperature protects plants from
heat damage by addressing the problems associated
with protein misfolding and aggregation (Queitsch et
al．，2000)． We compared the Fv /Fm in wild-type
A. thaliana (Col-0)with that in an HSP101-defi-
cient mutant (hot-1)after 4 h at 42 ℃ and during
the subsequent recovery process at 22 ℃ to deter-
mine whether HSP101 helps to protect plays a role
in the photochemical apparatus (Fig. 4A)． After
heat shock，Fv /Fm declined to about 0. 2 in both
plants． The difference of Fv /Fm between the two
plants became increasingly pronounced after 4 days
of recovery． This result demonstrated that HSP101
plays an important role in the photochemical repair
process in Arabidopsis． Next，we quantified HSP101
protein in the two plants after heat treatment and dur-
ing the subsequent recovery process to investigate
Fig. 4 Contribution of HSP101 to the photochemical recovery
process in A. paniculata and A. thaliana
A． The maximum quantum yield of PSII (Fv /Fm)in hot-1 and Col-0
of Arabidopsis after heat treatment (42 ℃，4 h)and during the subse-
quent recovery period． Solid (with squares)and dashed lines (with
circles)represent hot-1 and Col-0，respectively．“0. 25 d”means
0. 25 d of recovery at 22 ℃ after heat treatment，and so on;B． The
accumulation of HSP101 in A. paniculata and A. thaliana after 1 h of
heat treatment at 48 ℃ with acclimation and following recovery period．
“1 d”means 1 d of recovery at 22 ℃ after heat treatment，and so on
whether and how HSP101 contributes to the process
of photochemical recovery in A. paniculata (Fig. 4B)．
Although HSP101 was induced rapidly in both spe-
cies after heat treatment，it was rapidly degraded after
1 d of recovery in A. paniculata，but maintained a
high level of accumulation throughout the entire 4-
day recovery process in A. thaliana． This indicated
that the rapid induction of HSP101 in A. paniculata
might be a signal that initiates the photochemical re-
pair process but does not play a role in the subse-
quent recovery process in A. paniculata after moder-
ate heat treatment． This contrasts with changes in the
expression and likely role of HSP101 in A. thaliana
after its exposure to heat stress and its subsequent re-
covery．
2. 5 The high level of survival of A. paniculata
seedlings under severe heat stress was consistent
with its tolerance of moderate heat stress
To verify that the chlorophyll fluorescence was a
reliable indicator of the heat tolerance of A. paniculata
under a moderately high temperature，we compared
the survival of this species with that of A. thaliana
following more severe heat treatment． As shown in
Fig. 5，whereas the growth of A. paniculata seedlings
was healthy and normal，seedlings of A. thaliana
suffered from irreversible heat damage and became
etiolated after 3 h at 45 ℃ followed by 5 days of re-
covery at 22 ℃ ． This result reflected the substantial
heat tolerance of A. paniculata under an extremely
high temperature，which was consistent with its photo-
synthetic characterisation under moderate heat stress．
3 Conclusion
A. paniculata clearly showed strong heat toler-
ance under moderate stress． Compared with its rela-
tive A. thaliana，it presented greater photochemical
efficiency after exposure to a moderately high tem-
perature and more rapid repair of PSII． We also in-
vestigated certain physiological and biochemical fac-
tors to clarify the mechanism responsible for this rap-
id reversible change in photochemical efficiency of
A. paniculata under a moderately high temperature，
25 植 物 分 类 与 资 源 学 报 第 37卷
Fig. 5 Nine-day-old seedlings grown at 22 ℃ were exposed to 45 ℃ in the dark for 3 h，and were then returned to
22 ℃ for recovery． This photograph was taken after 5 days of recovery at room temperature
as experienced in the alpine environments that it in-
habits． Initially，the limited increase in F0 and more
significant increase in Fm during the recovery stage
were the factors that produced the rapid increase of
photochemical efficiency． The dramatic and transient
induction of Y(NPQ)dissipated excess energy to
protect the photosystem from heat damage and photo-
damage． Lastly but most importantly，the rapid and
transient pattern of response of HSP101 after heat
treatment initiated photochemical repair and ensured
that this process continued smoothly． In other words，
all of these traits contributed to the substantial heat
tolerance of A. paniculata，especially in terms of its
ability to continue to carry out photosynthesis under
moderate stress． This was consistent with the strong
thermotolerance of A. paniculata under extreme heat
stress，which failed to cause a high rate of lethality
in A. paniculata． Its heat tolerance system and rapid
photochemical repair may constitute adaptations that
enable A. paniculata to survive in alpine environments．
Investigation of how moderate heat stress is tolerated
could provide insights into how to make crops more
thermotolerant through genetic modifications．
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