全 文 ：饱和白光引起的光系统 II 捕光复合体 ( LHCII ) 从反应中心
复合体脱离不同于弱红光引起的状态 1 向状态 2 的转换
?
陈 悦1 ,2 , 许大全1
??
(1 中国科学院上海生命科学研究院植物生理生态研究所 , 上海 200032;
2 中国科学院研究生院 , 北京 100049 )
摘要 : 我们观测了不同光照预处理对拟南芥、小麦和大豆叶片光合作用和低温 ( 77K ) 叶绿素荧光参数
F685、 F735 和 F685?F735 的影响。野生型拟南芥叶片光合作用对饱和光到有限光转变的响应曲线是 V 型 ,
而缺乏叶绿体蛋白激酶的突变体 STN7 的这一曲线为 L 型。饱和白光可以引起拟南芥叶片 F685?F735 的明
显降低 , 但是 F735 没有明显增高 , 而弱红光可以导致拟南芥叶片 F685?F735 的明显降低和 F735 的明显增
高 , 表明弱红光可以引起状态 1 向状态 2 的转变 , 同时伴随从光系统 II 脱离的 LHC II 与光系统 I 的结合 ,
而饱和白光只能引起 LHC II 从光系统 II 反应中心复合体脱离。并且 , 低温叶绿素荧光分析结果证明 , 饱
和白光可以引起大豆叶片 LHC II 脱离 , 但是不能引起小麦叶片 LHC II 脱离 , 而弱红光可以引起小麦叶片
的这种状态转换 , 却不能引起大豆叶片的这种状态转换。因此 , 饱和白光引起的野生型拟南芥和大豆叶片
的 LHC II 脱离不是一个典型的状态转换现象。
关键词 : 拟南芥 ; 光系统 II 捕光复合体 (LHC II ) ; 低温 (77K ) 叶绿素荧光 ; 净光合速率 ; 可逆脱离 ; 状
态转换
中图分类号 : Q 945 文献标识码 : A 文章编号 : 0253 - 2700 (2009) 01 - 067 - 08
Dissociation of Photosystem II Light-harvesting Complex (LHC II )
from the Reaction Center Complex Induced by Saturating
White Irradiation Differs from the Transition from State
1 to State 2 Induced by Weak Red Irradiation
CHEN Yue1 , 2 , XU Da-Quan1 * *
( 1 Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences,
Shanghai 200032 , China; 2 Graduate University of Chinese Academy of Sciences, Beijing 100049 , China)
Abstract: The effects of different irradiance pre-treatments on leaf photosynthesis and low temperature ( 77K ) chlorophyll
fluorescence (LTCF) parameters F685 , F735 , and F685?F735 wereobserved in Arabidopsis, wheat, and soybean leav-
es . The curve of photosynthetic responsing to irradiance transition from saturating to limiting one in Arabidopsis wild-type
leaves was the V pattern, while thecurve in Arabidopsis mutant lacking chloroplast protein kinaseSTN7 was theL pattern .
Saturatingwhite irradiation (SWI ) could induce the significantly decreased F685?F735 without a significantly increased
F735 , while weak red irradiation (WRI ) could leadto the significantly declined F685?F735 witha significantly increased
F735 . The resultsshowedthat theattachment of dissociated LHC II to PS I in Arabidopsiswild-type leaves, indicatingthat
WRI can causethetransition fromstate1 to sate2 , whileSWI can only induceLHC II dissociation fromPSII reaction cen-
云 南 植 物 研 究 2009 , 31 (1) : 67～74
Acta Botanica Yunnanica DOI : 10 .3724?SP. J . 1143 .2009.08127
?
?? ?Author for correspondence; E-mail : dqxu@ sippe. ac. cn
Received date: 2008 - 06 - 23 , Accepted date: 2008 - 11 - 20
作者简介 : 陈悦 ( 1978 - ) 女 , 博士 , 主要从事光合作用研究。 ?
Foundation item: The National Basic Research Program of China ( Project No . 2005CB121106)
ter complex . Moreover theresults of LTCF analysis demonstrated that SWI could induce theLHC II dissociation in soybean
but not wheat leaves, whileWRI could causethe statetransition inwheat but not soybean leaves . HencetheLHC II disso-
ciation caused by SWI in Arabidopsiswild-type and soybean leaves was not a typical phenomenon of the state transition .
Key words: Arabidopsis; Light-harvestingcomplex of photosystem II (LHC II ) ; Low temperature (77K) chlorophyll fluo-
rescence; Net photosynthetic rate; Reversible dissociation; State transition
The largest efficiency of photosynthesis depends
on the cooperation of the photosystem II ( PS II ) and
photosystem I (PS I ) , while the cooperation relies on
the balanced distribution of excitation energy between
the two photosystems . However, due to the difference
in radiation absorption property between the two photo-
systems and the change in quality of sunlight reaching
the photosynthetic apparatus at different time during
day, the received excitation energy is often unbalanced
between the two photosystems . State transitions provide
a mechanism whereby more balanced excitation of the
two photosystems can be achieved ( Fork and Satoh,
1986; Niyogi , 1999; Haldrup et al. , 2001) .
The state transition initially discovered by Murata
(1969 ) andBonaventura and Myers ( 1969) is involved
in a reversible associationof some light-harvesting com-
plex II ( LHC II ) with either PSII or PSI . During the
transition fromstate 1 to 2 , someLHC IIs arephospho-
rylated, migrate to unstacked thylakoids, and attach to
PS I ( Bassi et al. , 1988; Vallon et al. , 1991; Allen,
1992; Samson andBruce, 1995; Horton et al. , 1996;
Gal et al. , 1997; Tan et al. , 1998; Lunde et al. ,
2000; Snyders and Kohorn, 2001 ) . In reverse, these
phosphorylated LHC IIs aredephosphorylated, return to
stacked thylakoids, and re-attach to PS II when trans-
lating from state 2 to 1 . In these events, the protein
kinase Stt7 or STN7 is required for LHC II phosphory-
lation and state transition (Depège et al. , 2003; Bel-
lafiore et al. , 2005) .
Similar to state transitions, the reversible dissoci-
ation of someLHC IIs induced by saturating irradiance
(SI ) (Hong and Xu, 1999; Chen and Xu, 2006 ) is
also involved in LHC II phosphorylation and dissocia-
tion fromPSII core complex (Allen et al. , 1981; Ben-
nett, 1991; Harrison and Allen, 1991; Allen, 1992;
McCormac et al. , 1994; Wollman, 2001) . Then, the
questions rise: whether or not the reversible LHC II
dissociation caused by SI is the same as state transi-
tion? If not so, what is thedifferencebetween them? In
order to answer these questions, the effects of different
radiation (saturating white irradiation, SWI , and weak
red irradiation, WRI ) pre-treatment on leaf photosyn-
thesis and low temperature ( 77K ) chlorophyll fluores-
cence parameters were observed in Arabidopsis, soy-
bean and wheat .
Materials and Methods
Plant growth
The potted plants of soybean ( Glycine max, cv . Baim-
angjie) , wheat ( Triticumaestivum, cv . Gaoyuan602) , and Ar-
abidopsis ( Arabidopsis thaliana, cv . Columbia) including the
mutant stn7 offered by Dr . Vera Bonardi ( Botanisches Institut,
Development Biologie I , Ludwig-Maximilians- Universit?t, Ger-
many) and its wild type were grown in the phytotrons with 25?
20℃ ( day?night) and a photosynthetic photon flux density
(PPFD) of about 300μmol m- 2 s- 1 ( 12 h?12 h light-dark cy-
cle) for soybean and wheat or with 22℃ ( day and night) and a
PPFD of about 100μmol m- 2 s- 1 (9 h?15 h light-dark cycle) for
Arabidopsis . The plants were irrigated everyday to avoid water
stress . Experiments were performed using fully expanded and
healthy leaves .
Leaf irradiation and photosynthesis measurement
The plant leaveswerefirst illuminated by limiting irradiance
(LI : 300μmol m- 2 s- 1 ) until net photosynthetic rate ( Anet)
reached a steady state . Then, the limiting irradiance was re-
placed by saturating irradiance (SI : 750μmol m- 2 s - 1 , LI-SI )
for photosynthesis . After Anet rose gradually to a new steady
statethe irradiance was reduced back to limiting one ( LI-SI-LI )
until Anet reachedagaina steady state . In general , Anet reaches
itssteady state value after about 15 and 30 minutes of illumina-
tion at limiting and saturating irradiance, respectively . Anet was
measured in situ at 350μmol CO2 mol - 1 by aportable photosyn-
thetic gas analysis systemLI-COR 6400 with a LED light source
(LI-COR Inc . Lincoln, Nebraska, USA) .
Accordingto the procedure of irradiancechanges mentioned
above, theother leaveswere illuminatedby ametal halogen lamp
(1 000 W) . A flowing layer of water was placed between the
lamp and the leaves to remove heat . After illumination (LI and
LI-SI ) the leaves were immediately dropped into liquid nitrogen
86 云 南 植 物 研 究 31 卷
for low-temperature (77K ) chlorophyll fluorescence analysis .
Fully dark-adapted leaves were illuminated by WRI ( 650
nm, 20μmol photons m- 2 s- 1 ) for 20 min . The weak red radi-
ation was obtained using an interference filter with a half wave-
length width of 10 nm . After illumination these leavesweredark-
adaptedfor 30 s and then put into liquid nitrogen for the 77K
chlorophyll fluorescence analysis .
Low temperature chlorophyll fluorescence analysis
Low-temperature chlorophyll fluorescence was analyzed at
77K with a44 W-fluorescence spectrofluorimeter built in our lab-
oratory . F685 , F735 and F685?F735 were measured and cal-
culated as previously described (Hong and Xu, 1999 ) .
Statistical analysis
Statistical analysis of all data including mean, standard er-
ror, and t-tests was made with Sigma Plot 8 .0 ( SPSS, Inc .
USA) .
Results
Photosynthetic response of Arabidopsis leaves to the
change in irradiance
When irradiance was changed fromsaturating (750
μmol m- 2 s- 1 ) to limiting one ( 300 μmol m- 2 s- 1 ) ,
Anet in Arabidopsis wild-type leaves declined immedi-
ately to a value lower than that at limiting irradiance
before saturating irradiation . Then, Anet roseslowly to
a stable value near to that at limiting irradiance before
saturating irradiation ( Fig. 1 : a) . However, the re-
sponses of Anet in Arabidopsis mutant stn7 lacking
chloroplast protein kinase STN7 to the irradiance tran-
sition were significantly different from those in Arabi-
dopsis wild-type leaves . After irradiance was changed
from saturating to limiting one, Anet in the mutant
stn7 leaves decreased immediately to a stable value
similar to that before saturating irradiation, namely, no
slow rise followed the sharp drop in Anet (Fig. 1 : b) .
These results indicate that the photosynthetic response
curves to irradiance transition fromsaturatingto limiting
one in Arabidopsis wild-type and mutant stn7 leaves
are the V and L patterns, respectively .
Effects of saturating white irradiation pretreatment
on 77K chlorophyll fluorescence parameters in Ar-
abidopsis leaves
The 77K chlorophyll fluorescenceparameters F685
and F685?F735 declined significantly, but F735 had
no significant change in Arabidopsis wild-type leaves
pre-illuminated by saturating white irradiation, com-
pared with those in leaves pre-illuminated by limiting
white irradiation ( Fig. 2 : a) . Nevertheless, in Arabi-
dopsis mutant stn7 leave no significant change was ob-
served in F685 and F685?F735 (Fig. 2 : b) .
Effects of weak red irradiation pretreatment on
77K chlorophyll fluorescence parameters in Arabi-
dopsis leaves
The 77K chlorophyll fluorescenceparameters F685
and F685?F735 decreased significantly and F735 in-
creased markedly in Arabidopsiswild-type leaves pre-il-
Fig . 1 Responseof net photosynthetic rate ( Anet) in Arabidopsis leaves to change in irradiance
(a) Wild type; ( b) Mutant stn7 . LI : limiting irradiance (300μmolm- 2 s - 1 ) ; SI : saturating irradiance (750μmolm- 2 s- 1 ) .
Each value in this figure is the mean of three leaves with standard error expressed as a vertical bar
961 期 CHEN and XU: Dissociation of Photosystem II Light-harvesting Complex (LHC II) fromthe Reaction . . .
Fig . 2 Changes in 77K chlorophyll fluorescence parameters F685 , F735 , and F685?F735 of Arabidopsis
leaves caused by pre- illumination with saturating irradiance
(a) Wild type; ( b) Mutant stn7 . In this figure the parameter values are expressed as thepercentages of limiting irradiance (LI , 300μmolm- 2 s- 1 )
-pre- illuminated leaves, and each value is the mean of 3 - 4 repeats with standard error expressed as a vertical bar . LI : limiting irradiance
(300μmolm- 2 s- 1 ) ; SI : saturating irradiance ( 750μmolm- 2 s - 1 ) . Asterisks * and * * indicate respectively significant ( p< 0 .05 )
and very significant ( p< 0 .01 ) differences between SI-pre- illuminated and LI-pre- illuminated leaves
luminated byweak red irradiation, compared with those
of dark control leaves (Fig. 3 : a) . However, nosignif-
icant change in these parameters was observed in the
mutant stn7 leaves pre-illuminated by weak red irradi-
ation (Fig. 3 : b) .
Changes in 77K chlorophyll fluorescence parame-
ters in soybean leaves induced by weak red irradi-
ation or saturating white irradiation pretreatment
Compared with dark control or pre-illumination
with limiting white irradiation, pre-illumination with
weak red irradiation or saturating white irradiation led
tosignificant decreases in F685 and F685?F735 with-
out significantly increased F735 in soybean leaves
(Fig. 4 : a, b) , indicating that neither saturatingwhite
irradiation nor weak red irradiation can cause the tran-
sition fromstate 1 to state 2 .
Changes in 77K chlorophyll fluorescence parame-
ters in wheat leaves induced by pre-illumination
with weak red irradiation or saturating white irra-
diation
Inwheat leaves thepre-illumination with weak red
irradiation led to significantly decreased F685 and
Fig . 3 Changes in 77K chlorophyll fluorescence parameters F685 , F735 , and F685?F735 of Arabidopsis
leaves caused by pre- illumination with weak red irradiation
(a) Wild type; ( b) Mutant stn7 . In this figure theparameter values are expressed as the percentages of dark control leaves,
and each value is the mean of 3 - 4 repeats with standard error expressed as a vertical bar . Asterisk * indicates that
differences betweenweak red irradiation-pre-illuminated and dark control leaves are significant ( p< 0 .05)
07 云 南 植 物 研 究 31 卷
Fig . 4 Changes in 77K chlorophyll fluorescence parameters F685 , F735 , and F685?F735 of
soybean leaves caused by pre-illumination with weak red irradiation
( a, 20μmolm- 2 s - 1 ) or saturatingwhite irradiation ( b, SI , 750μmolm- 2 s - 1 ) . In this figure the parameter values are expressed as the percentages
of dark control leaves ( a) or limiting irradiance (LI , 300μmolm- 2 s- 1 ) -pre- illuminated leaves (b) , and each value is the mean of 3 - 4
repeats with standard error expressed as a vertical bar . Asterisk * indicates that the differences between weak red irradiation-pre-
illuminated and dark control leaves or between SI -pre- illuminated and LI-pre-illuminated leaves are significant ( p< 0 .05 )
Fig . 5 Changes in 77K chlorophyll fluorescenceparameters F685 , F735 , and F685?F735 of wheat leaves caused by pre- illumination
with weak red irradiation ( a, 20μmolm- 2 s - 1 ) or saturatingwhite irradiation ( b, SI , 750μmolm- 2 s - 1 ) .
In this figure the parameter values are expressed as the percentages of dark control ( a) or limiting white irradiation (LI , 300μmolm- 2 s - 1 )
-pre- illuminated ( b) leaves, and each value is the mean of 3 - 4 repeats with standard error expressed as avertical bar .
Asterisks * and * * indicate respectively significant ( p< 0 . 05) and very significant ( p< 0 .01 )
differences between weak red irradiation-pre-illuminated and dark control leaves or between
SI -pre- illuminated and LI -pre- illuminated leaves
F685?F735 accompanied by remarkably increased
F735 ( Fig. 5 : a) . However, the pre-illumination with
saturatingwhiteirradiation couldnot inducesuch chang-
es in these parameters (Fig. 5: b) , indicating that weak
red irradiation rather than saturating white irradiation
can induce the transition fromstate 1 to state 2 .
Discussion
Using agenetic approach it has demonstrated that
the chloroplast thylakoid-associated serine-threonine
protein kinase, Stt7 , is required for the phosphoryla-
tion of LHC II and for state transition in Chlamydo-
monas (Depège et al. , 2003 ) . Similarly, it has been
shown that Arabidopsis mutant stn7 lacking chloroplast
protein kinaseSTN7 cannot performLHC II phosphory-
lation and state transition ( Bellafiore et al. , 2005 ) .
Based on the V pattern of leaf photosynthetic response
curve in Arabidopsis wild type ( Chen and Xu, 2006) ,
171 期 CHEN and XU: Dissociation of Photosystem II Light-harvesting Complex (LHC II) fromthe Reaction . . .
it is supposed that the curve of its mutant stn7 should
be the L pattern . The experimental results reported
here ( Fig. 1 ) confirm this supposition, providing new
evidence for SI-induced reversible dissociation of some
LHC IIs from the PSII reaction center complex . The L
pattern of the photosynthetic response curve in Arabi-
dopsismutant stn7 isobviously due toSTN7 loss block-
ing the phosphorylation of LHC II and whereby dissoci-
ationof LHC II fromthe PS II core complex . Thesatu-
rating irradiation-caused some LHC IIs dissociation
from the PSII in Arabidopsis wild type suggests that
STN7 isnot inactivated at saturating irradiation . This is
not consistent with that theprotein kinaseStt7 required
for LHC II phosphorylation is inactivated at high irradi-
ation reported by Rintam?ki et al. ( 2000 ) . Whether
this contradiction originates from different tolerance to
high irradiation of STN7 and Stt7 fromdifferent species
( higher plant and green alga) is worth studying .
The reversible dissociation of LHC II induced by
illuminationwith saturating irradiation, weobserved, is
not a phenomenon of state transitions . There are some
important differences between the two things .
First, they had different mechanic characteristics
for LHCIIs dissociation from PSII reaction center com-
plex .Thestatetransition fromstate1 to state 2 is char-
acterized not only by the dissociationof LHC II fromPS
II but also by themigration and attachment of dissociat-
ed LHC II to PS I (Bassi et al. , 1988; Vallon et al. ,
1991; Allen, 1992; Samson and Bruce, 1995; Horton
et al. , 1996; Gal et al. , 1997; Tan et al. , 1998;
Lunde et al. , 2000; Snyders and Kohorn, 2001 ) .
Lunde et al. ( 2000 ) have excellently demonstrated
that not only doesLHC II functionally connect to PSI in
state 2 , but also this connection is essential for state
transition . At 77K the chlorophyll fluorescence emis-
sions peaked at 685 nm ( F685) and 735 nm ( F735)
stemfrom PS II and PS I antennae, respectively . Al-
though F685 comes from the core antenna of PS II
(Bassi et al. , 1990; Krause and Weis, 1991 ) , the
peripheral antenna LHC II alsocontributes to F685 be-
causephotons absorbed by LHC II can betransferred to
the core antennawhen they are linked to eachother . A
change in F685 or F735 , therefore, can reflect the
change in the status of association of LHC II and PS II
core complex or LHCII and PSI core complex, respec-
tively . In the study reported here the pre-illumination
with saturating irradiation led to decreased F685 and
F685?F735 without increased F735 in Arabidopsis
wild type (Fig. 2 : a) . Therefore, the saturating irradi-
ation-induced dissociation of LHC II , as shown by the
decreased F685 and F685?F735 , is not a phenome-
non of state transition (fromstate1 to state 2) because
the dissociated LHCII did not attach PSI , as shown by
the unchanged F735 (Fig. 2: a) .
Second, they are induced by different irradiation
factors . The results reported here showed that the pre-
illumination with weak red irradiation could cause the
decreases in F685 and F685?F735 and increase in
F735 , indicatingtheoccurrenceof state transition from
state 1 to state 2 in Arabidopsis wild type (Fig. 3) and
wheat (Fig. 5 : a) . However, that the pre-illumination
with saturating white irradiation could not induce such
changes in these chlorophyll fluorescence parameters,
indicating no occurrence of the state transition in Ara-
bidopsis wild type (Fig. 2 : a) and wheat (Fig. 5 : b) .
Obviously, the inductionof LHC II dissociation and the
state transition depends on different irradiation, satu-
rating white irradiation and weak red irradiation, re-
spectively . Also, thestate transition is induced only by
low irradiation rather than high irradiation (Walter and
Horton, 1991; Lunde et al. , 2002) .
Third, they perform different functions . The re-
versibleLHC II dissociation caused by saturating illu-
mination is a protective strategy from photodamage of
the PS II reaction centers ( Zhang and Xu, 2003 ) ,
while statetransitions serve to balance excitation energy
distribution of the two photosystems ( Fork and Satoh,
1986; Niyogi , 1999; Haldrup et al. , 2001; Kruse,
2001) . The contribution of statetransition is quite lim-
ited in protecting the photosynthetic apparatus from
photodamage, and the protective role is much smaller
than thexanthophylls cycle- and△pH across thylakoid
membrane-dependent energy dissipation processes
( Fork et al. , 1986; Demmig-Adams and Adams,
1992; Shen et al. , 1996; Hong and Xu, 1999; Hong
et al. , 1999; Demming-Adams, 2003 ) .
27 云 南 植 物 研 究 31 卷
Fig . 6 Schematic model describing the differences between reversible LHC II dissociation induced by irradiance change
and state transition induced by radiation quality change
PSII : photosystemII reaction center complex; PSI : photosystem I reaction center complex; LHC II : PS II light-harvesting complex; LHCI : PS I
light-harvesting complex; hv: radiation energy . The arrows between two complexes indicate the direction of radiation energy transport
Main differences in induction irradiation, charac-
teristics, and function between the reversible dissocia-
tion of LHC II and state transition are summarized in
Fig. 6 .
Surprisingly, the weak red irradiation could in-
duce significant decreases in F685 and F685?F735
but not cause a remarkable increase in F735 of soy-
bean leaves ( Fig. 4 : a) , indicating that the LHC II
dissociation from PS II is not followed by the attach-
ment of dissociated LHC II to PS I , namely, notypical
state transition fromstate 1 to state 2 occurs in soybean
leaves . Perhaps under theirradiation absorbed predom-
inantly by PS II soybean leaves are able to balance ex-
citation energy distribution between the two photosys-
tems only by LHC II dissociation fromPS II without at-
tachment of dissociated LHC II to PS I andwhereby de-
crease in radiation absorption of PS II . Whether the
supposition is correct or not ? What controls the attach-
ment of dissociated LHC II to PS I ? Further studies are
required to answer these questions .
Acknowledgments: We thank Dr . Vera Bonardi for offering
seeds of the Arabidopsis mutant stn7 .
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