Document Text Contents
Page 2
The Chloroplast
Page 226
Yuki Nakamura et al.
for Type A function and what it would be like if
MGD1 was completely eliminated. Moreover, it
was still uncertain whether MGDG is essential for
chloroplast function. To address this question, we
recently isolated and characterized a null mutant
of MGD1, designated mgd1-2, obtained from an
available T-DNA tagged mutant line (Kobayashi
et al., 2007). When the siliques of mgd1/MGD1
heterologous mutant were examined, about 25%
of the embryos were aberrant, suggesting that these
seeds may be mgd1-2/mgd1-2 homozygous with a
likely embryonic lethal phenotype. Interestingly,
however, when the wrinkled seed were planted,
they germinated. The phenotype of mgd1-2 was
intriguing; the mutant plant was very small and
white compared to WT. Lipid analyses of mgd1-2
revealed that plastidic membrane lipids, such as
MGDG, DGDG, and sulfoquinovosyldiacylglyc-
erol (SQDG), were hardly detectable, presumably
due to the deficiency in chloroplasts formation.
Indeed, an observation of mutant chloroplasts by
electron microscopy showed a disrupted structure
of thylakoid membranes. Thus, results of analy-
ses with mgd1 (referred to as mgd1-1 hereafter)
and mgd1-2 indicated that MGD1 is responsible
for the bulk of MGDG synthesis and cannot be
replaced by Type B MGDG synthases. Therefore,
its function is indispensable for photosynthetic
ability and formation of proper chloroplasts.
As for type B MGD (MGD2 and MGD3),
preliminary results of mutant analyses showed
no significant impact on lipid metabolism in
photosynthetic organs, although analyses in non-
photosynthetic organs are still ongoing. Since
Awai and co-workers showed that MGD2 and
MGD3 were expressed in different organs (Awai
et al., 2001; Kobayashi et al., 2004), it is of great
interest to find out whether these two isozymes
are functionally redundant or have distinct
functions each other (Fig. 1).
V Substrate Supply Systems
for MGDG Synthesis
The substrates for MGDG synthesis are DAG
and UDP-Gal. Here, our focus is on the supply of
DAG for MGDG biosynthesis. DAG is supplied
by multiple metabolic pathways, and production
of DAG itself presents a complex problem as this
lipid class serves as substrate for galactolipids,
phospholipids and even triacylglycerol (TAG).
For the enzymes involved in the biosynthesis of
DAG and its precursors, readers are referred to
Fig. 1. Physiological functions of type A and type B MGDs for plant growth. Type A MGD1 are expressed widely in photosyn-
thetic tissues. By contrast, Type B MGD2 and 3 showed intense expression particularly in non-photosynthetic tissues during Pi
starvation and pollen tube growth.
Photosynthetic tissues Non-photosynthetic tissues
Embryogenesis
Photosynthetic
membrane
construction
Pollen tube growth
Pi-stress response in the root
Type A
(atMGD1)
Type B
(atMGD2,3)
192
Page 227
13 Biosynthesis and Function of MGDG
Joyard et al. (1998). The biosynthesis of MGDG
occurs exclusively in plastids (Douce and Joyard,
1980). However, DAG is known to be supplied
either within plastids (prokaryotic pathway) or by
way of the ER (eukaryotic pathway) (Roughan
and Slack, 1982). Early studies suggested that
in both pathways, DAG is derived from differ-
ent lipid precursors. In the prokaryotic pathway,
DAG is produced from phosphatidic acid (PA) by
PA phosphatase (PAP) (Joyard and Douce, 1977).
On the other hand, eukaryotic DAG is generally
assumed to be derived from PC synthesized in the
ER (PC hypothesis). This hypothesis is based on
in situ pulse chase studies, where radiolabel tran-
siently allocated to the cellular pool of PC being
incorporated mainly into MGDG (Roughan, 1970;
Heinz, 1977; Douce and Joyard, 1980; Roughan
and Slack, 1982). This hypothesis involves (1) the
synthesis of PC, (2) its transfer (or that of DAG)
to chloroplasts, and (3) the integration of the DAG
backbone into MGDG and DGDG. Although
the transport manner and the transported lipid
have not been identified yet, lysoPC (A. porrum;
Mongrand et al., 1997, 2000), DAG (B. napus;
Williams et al., 2000) and PA (A. thaliana; Xu
et al., 2005; Awai et al., 2006b) have been pro-
posed recently as the possible transported lipid.
An early study showed the possibility that PC
could be the transported lipid: when spinach chlo-
roplasts were pre-incubated with [14C]-containing
liposomes and phospholipid transfer proteins prior
to incubation with phospholipase C (PLC) and
UDP-Gal, formation of [14C]MGDG was observed
(Oursel et al., 1987). Recently, Jouhet and co-
workers reported with suspension culture of A.
pseudoplatanus that, during phosphate starved
conditions which activate galactolipid biosynthe-
sis, a transient increase of PC was followed by its
rapid decrease and concomitant increase in DAG
(Jouhet et al., 2003). Furthermore, the fatty acid
composition of PC and DAG were very similar,
suggesting that DAG is supplied by the hydroly-
sis of PC. Another report by Andersson and co-
workers who studied the conditions that would
allow the conversion of chloroplast-localized PC
into the precursor for MGDG synthesis showed
that cytosolic phospholipase D (PLD) activity that
resides in the >100kDa fraction is involved in the
substrate supply for MGDG synthesis (Anders-
son et al., 2004). Since PLD reaction gives rise
to PA, subsequent reaction by PAP should be
coupled to the reaction. This idea of the combina-
tory two-step reaction seems somewhat irrational,
but the involvement of activity for direct hydrol-
ysis by a PC-hydrolyzing PLC (PC-PLC) is not
clear even though the activity itself was reported
in several studies (Kates, 1955; Strauss et al.,
1976; Chrastil and Parrish, 1987; Rouet-Mayer
et al., 1995; Scherer et al., 2002). However, sig-
nificant progress has been made in recent 3 years
with Arabidopsis for identifying and characteriz-
ing key enzymes involved in this mechanism. As
mentioned earlier, Arabidopsis has the machinery
for MGDG synthesis both at the outer and inner
envelope membrane of chloroplast. Because these
two pathways are separated from each other (Ben-
ning and Ohta, 2005), the DAG supply for these
two pathways could rely on independent enzymes/
mechanisms (Fig. 2).
A DAG Supply to the Outer Envelope
Outer envelope-localized MGDG synthesis does
not contribute to the bulk of MGDG synthesis
under normal growth condition (Benning and Ohta,
2005). Therefore, the outer envelope-specific flux
is often masked by the inner envelope-localized
pathway, and therefore it is difficult to estimate
the contribution of the outer envelope system
(Benning and Ohta, 2005). It was reported that
phosphate starvation activates specifically the
outer envelope-localized pathway. Our group made
use of this condition to identify which metabolic
pathway is activated for DAG supply (Nakamura
et al., 2005). Hydrolysis of PC to yield DAG is
shown to be highly induced upon Pi starvation, and
moreover, inhibition of PLD activity by n-BuOH
showed no significant decrease in the activity,
suggesting that the DAG supply from PC is medi-
ated by one-step hydrolysis of PC-PLC. Based on
homology search using known bacterial PC-PLCs,
six putative PC-PLCs were detected in Arabidop-
sis and designated non-specific phospholipase C
(NPC). Expression studies revealed that one of
them, NPC4, was strongly induced upon Pi star-
vation. In vitro enzyme assays of recombinant
NPC4 showed significant PLC activity for PC and
phosphatidylethanolamine (PE) but not phosphati-
dylinositol (PI) or PA. Its subcellular localization
using a specific anti- NPC4 antibody was con-
firmed to be in the plasma membrane. Two inde-
pendent T-DNA lines giving rise to npc4 knock
193
Page 452
Subject Index
Synechocystis, 21, 41, 42, 44–46, 62, 63, 66, 109,
86, 159–163, 165, 177, 196, 197, 204,
386, 388, 390, 391
Synechocystis PCC6803, 42, 46, 62, 63, 159,
177, 196
T
tAPX gene network, 337, 339
Taxol, 96, 121, 122, 128
Terpenes
biosynthesis, 102, 105, 140, 141, 143
diterpenes, 96, 101, 105, 113, 114, 128,
140, 149
monoterpenes, 96, 101, 105, 110, 113,
114, 120, 122, 128, 140–144,
148, 149
sesquiterpenes, 96, 101, 102, 105, 106, 113,
120, 128, 140–143, 148
Tetrapyrroles, 7, 10–21, 27, 30, 32, 39–49, 63, 208,
217, 218, 400–404
Therapeutic proteins, 263, 264, 272, 273,
277, 278
Thermal dissipation, 348–350, 352, 353,
355–356
Thermoluminescence, 406
Thermosynechococcus elongatus, 86, 176, 206,
383
Thin layers of silica gel H, 29
Thioredoxin, 42, 187, 326, 382, 390–391
Thylakoid
apoproteins, 8–9, 11–12
biogenesis, 213–226
membrane, 7, 9, 11, 12, 32, 40, 63, 69–73,
148, 159, 172, 174, 175, 177–180,
189, 191, 192, 205, 208, 214, 222,
224, 232, 238, 239, 241, 254, 326,
352, 353, 356, 357, 367, 368, 373,
382, 383, 386, 400–406
Tobacco, 42, 44, 45, 59, 67, 72, 102, 113, 121,
122, 127–134, 161, 163, 177, 197, 246,
250–253, 255, 257, 263, 265–267, 269,
271–279, 285–303, 309, 310, 316, 320,
352, 354, 382, 386, 388, 389, 407, 408
BY-2 cells, 127–134
plastome, 251, 287–290, 302, 303
Tocochromanols, 155–166
Tocopherol, 121, 122, 155–166, 383–388, 402
level of, 112, 158
localisation, 96
Tocotrienol, 155–166
Transformation, 64, 251–254, 256, 257, 264,
267–275, 278–280, 287, 290, 292, 300,
302, 303, 309, 313, 314, 316, 320, 354,
374, 407
Transgene, 123, 252, 253, 257, 263, 264, 267–275,
279, 289, 291, 293, 314
cassette, 267, 269, 270
containment, 253, 257, 263, 267, 275
Transition dipoles, 12
Translation efficiency, 254, 298
Transmembrane electron transport, 370
Transplastomic, 251–257, 270–272, 274, 279,
280, 288, 290-296, 298
Trigalactosyldiacylglycerol (TGDG), 196, 205
Tropospheric ozone, 324, 325, 327, 331
Tyrosine, 62, 157, 160, 163, 289, 334
U
Ubiquinone, 96, 101, 102, 120, 128
biosynthesis, 101, 102, 120
localisation, 96
UDP-sulfoquinovose (UDP-SQ), 175, 176, 179
Unfolded state, 8–10, 20
Uridine-diphosphate-galactose (UDP-Gal),
186–188, 192, 193, 205, 208
Uroporphyrin III, 408
V
Vaccine antigens, 263–265, 269, 272, 273,
275–277
4VChlR. See 4-Vinyl Chl a reductase
4VCR. See 4-Vinyl chlorophyllide a reductase
4-Vinyl Chl a reductase (4VChlR), 8, 28, 35
4-Vinyl chlorophyllide a reductase (4VCR), 8,
28–36
Vinyl groups, 27, 58
[4Vinyl] Mg-protoporphyrin monoester reductase
(4VMpeR), 29–31, 34–37
[4-Vinyl] Mg-proto reductase (4VMPR), 8,
28–31, 35
4-Vinyl Pchlide a reductase (4VPideR),
8, 27–36
[4-vinyl] reductase (4VR), 8, 26–35
Violaxanthin, 232, 350, 384, 387, 402
Violaxanthin de-epoxidase, 350, 384, 387
Vitamin B3, 33
Vitamin B6, 402, 407
Vitamin E, 112, 114, 155–166
Vitamin K, 4, 112, 165
422
Page 453
Subject Index
(4VMpeR). See [4Vinyl] Mg-protoporphyrin
monoester reductase
4VMPR. See [4-Vinyl] Mg-proto reductase
4VPideR. See 4-Vinyl Pchlide a reductase
4V-Proto, 34
4VR isoforms, 28
W
Walker B motif, 41, 80, 81
Water soluble chlorophyll
binding proteins, 402
Water water cycle, 348, 349, 351–352,
356, 391, 392
Wave number, 16–17
Wild watermelon, 363–374
X
Xantha−F, 43, 79, 80, 85
Xantha−H gene, 80
Xanthophyll cycle, 60, 112, 207, 350, 387
Xanthophylls, 220, 222, 386, 387, 402
Xerophytes, 363–374
Z
Zeaxanthin, 112, 207, 350, 384, 387, 399, 402
423
The Chloroplast
Page 226
Yuki Nakamura et al.
for Type A function and what it would be like if
MGD1 was completely eliminated. Moreover, it
was still uncertain whether MGDG is essential for
chloroplast function. To address this question, we
recently isolated and characterized a null mutant
of MGD1, designated mgd1-2, obtained from an
available T-DNA tagged mutant line (Kobayashi
et al., 2007). When the siliques of mgd1/MGD1
heterologous mutant were examined, about 25%
of the embryos were aberrant, suggesting that these
seeds may be mgd1-2/mgd1-2 homozygous with a
likely embryonic lethal phenotype. Interestingly,
however, when the wrinkled seed were planted,
they germinated. The phenotype of mgd1-2 was
intriguing; the mutant plant was very small and
white compared to WT. Lipid analyses of mgd1-2
revealed that plastidic membrane lipids, such as
MGDG, DGDG, and sulfoquinovosyldiacylglyc-
erol (SQDG), were hardly detectable, presumably
due to the deficiency in chloroplasts formation.
Indeed, an observation of mutant chloroplasts by
electron microscopy showed a disrupted structure
of thylakoid membranes. Thus, results of analy-
ses with mgd1 (referred to as mgd1-1 hereafter)
and mgd1-2 indicated that MGD1 is responsible
for the bulk of MGDG synthesis and cannot be
replaced by Type B MGDG synthases. Therefore,
its function is indispensable for photosynthetic
ability and formation of proper chloroplasts.
As for type B MGD (MGD2 and MGD3),
preliminary results of mutant analyses showed
no significant impact on lipid metabolism in
photosynthetic organs, although analyses in non-
photosynthetic organs are still ongoing. Since
Awai and co-workers showed that MGD2 and
MGD3 were expressed in different organs (Awai
et al., 2001; Kobayashi et al., 2004), it is of great
interest to find out whether these two isozymes
are functionally redundant or have distinct
functions each other (Fig. 1).
V Substrate Supply Systems
for MGDG Synthesis
The substrates for MGDG synthesis are DAG
and UDP-Gal. Here, our focus is on the supply of
DAG for MGDG biosynthesis. DAG is supplied
by multiple metabolic pathways, and production
of DAG itself presents a complex problem as this
lipid class serves as substrate for galactolipids,
phospholipids and even triacylglycerol (TAG).
For the enzymes involved in the biosynthesis of
DAG and its precursors, readers are referred to
Fig. 1. Physiological functions of type A and type B MGDs for plant growth. Type A MGD1 are expressed widely in photosyn-
thetic tissues. By contrast, Type B MGD2 and 3 showed intense expression particularly in non-photosynthetic tissues during Pi
starvation and pollen tube growth.
Photosynthetic tissues Non-photosynthetic tissues
Embryogenesis
Photosynthetic
membrane
construction
Pollen tube growth
Pi-stress response in the root
Type A
(atMGD1)
Type B
(atMGD2,3)
192
Page 227
13 Biosynthesis and Function of MGDG
Joyard et al. (1998). The biosynthesis of MGDG
occurs exclusively in plastids (Douce and Joyard,
1980). However, DAG is known to be supplied
either within plastids (prokaryotic pathway) or by
way of the ER (eukaryotic pathway) (Roughan
and Slack, 1982). Early studies suggested that
in both pathways, DAG is derived from differ-
ent lipid precursors. In the prokaryotic pathway,
DAG is produced from phosphatidic acid (PA) by
PA phosphatase (PAP) (Joyard and Douce, 1977).
On the other hand, eukaryotic DAG is generally
assumed to be derived from PC synthesized in the
ER (PC hypothesis). This hypothesis is based on
in situ pulse chase studies, where radiolabel tran-
siently allocated to the cellular pool of PC being
incorporated mainly into MGDG (Roughan, 1970;
Heinz, 1977; Douce and Joyard, 1980; Roughan
and Slack, 1982). This hypothesis involves (1) the
synthesis of PC, (2) its transfer (or that of DAG)
to chloroplasts, and (3) the integration of the DAG
backbone into MGDG and DGDG. Although
the transport manner and the transported lipid
have not been identified yet, lysoPC (A. porrum;
Mongrand et al., 1997, 2000), DAG (B. napus;
Williams et al., 2000) and PA (A. thaliana; Xu
et al., 2005; Awai et al., 2006b) have been pro-
posed recently as the possible transported lipid.
An early study showed the possibility that PC
could be the transported lipid: when spinach chlo-
roplasts were pre-incubated with [14C]-containing
liposomes and phospholipid transfer proteins prior
to incubation with phospholipase C (PLC) and
UDP-Gal, formation of [14C]MGDG was observed
(Oursel et al., 1987). Recently, Jouhet and co-
workers reported with suspension culture of A.
pseudoplatanus that, during phosphate starved
conditions which activate galactolipid biosynthe-
sis, a transient increase of PC was followed by its
rapid decrease and concomitant increase in DAG
(Jouhet et al., 2003). Furthermore, the fatty acid
composition of PC and DAG were very similar,
suggesting that DAG is supplied by the hydroly-
sis of PC. Another report by Andersson and co-
workers who studied the conditions that would
allow the conversion of chloroplast-localized PC
into the precursor for MGDG synthesis showed
that cytosolic phospholipase D (PLD) activity that
resides in the >100kDa fraction is involved in the
substrate supply for MGDG synthesis (Anders-
son et al., 2004). Since PLD reaction gives rise
to PA, subsequent reaction by PAP should be
coupled to the reaction. This idea of the combina-
tory two-step reaction seems somewhat irrational,
but the involvement of activity for direct hydrol-
ysis by a PC-hydrolyzing PLC (PC-PLC) is not
clear even though the activity itself was reported
in several studies (Kates, 1955; Strauss et al.,
1976; Chrastil and Parrish, 1987; Rouet-Mayer
et al., 1995; Scherer et al., 2002). However, sig-
nificant progress has been made in recent 3 years
with Arabidopsis for identifying and characteriz-
ing key enzymes involved in this mechanism. As
mentioned earlier, Arabidopsis has the machinery
for MGDG synthesis both at the outer and inner
envelope membrane of chloroplast. Because these
two pathways are separated from each other (Ben-
ning and Ohta, 2005), the DAG supply for these
two pathways could rely on independent enzymes/
mechanisms (Fig. 2).
A DAG Supply to the Outer Envelope
Outer envelope-localized MGDG synthesis does
not contribute to the bulk of MGDG synthesis
under normal growth condition (Benning and Ohta,
2005). Therefore, the outer envelope-specific flux
is often masked by the inner envelope-localized
pathway, and therefore it is difficult to estimate
the contribution of the outer envelope system
(Benning and Ohta, 2005). It was reported that
phosphate starvation activates specifically the
outer envelope-localized pathway. Our group made
use of this condition to identify which metabolic
pathway is activated for DAG supply (Nakamura
et al., 2005). Hydrolysis of PC to yield DAG is
shown to be highly induced upon Pi starvation, and
moreover, inhibition of PLD activity by n-BuOH
showed no significant decrease in the activity,
suggesting that the DAG supply from PC is medi-
ated by one-step hydrolysis of PC-PLC. Based on
homology search using known bacterial PC-PLCs,
six putative PC-PLCs were detected in Arabidop-
sis and designated non-specific phospholipase C
(NPC). Expression studies revealed that one of
them, NPC4, was strongly induced upon Pi star-
vation. In vitro enzyme assays of recombinant
NPC4 showed significant PLC activity for PC and
phosphatidylethanolamine (PE) but not phosphati-
dylinositol (PI) or PA. Its subcellular localization
using a specific anti- NPC4 antibody was con-
firmed to be in the plasma membrane. Two inde-
pendent T-DNA lines giving rise to npc4 knock
193
Page 452
Subject Index
Synechocystis, 21, 41, 42, 44–46, 62, 63, 66, 109,
86, 159–163, 165, 177, 196, 197, 204,
386, 388, 390, 391
Synechocystis PCC6803, 42, 46, 62, 63, 159,
177, 196
T
tAPX gene network, 337, 339
Taxol, 96, 121, 122, 128
Terpenes
biosynthesis, 102, 105, 140, 141, 143
diterpenes, 96, 101, 105, 113, 114, 128,
140, 149
monoterpenes, 96, 101, 105, 110, 113,
114, 120, 122, 128, 140–144,
148, 149
sesquiterpenes, 96, 101, 102, 105, 106, 113,
120, 128, 140–143, 148
Tetrapyrroles, 7, 10–21, 27, 30, 32, 39–49, 63, 208,
217, 218, 400–404
Therapeutic proteins, 263, 264, 272, 273,
277, 278
Thermal dissipation, 348–350, 352, 353,
355–356
Thermoluminescence, 406
Thermosynechococcus elongatus, 86, 176, 206,
383
Thin layers of silica gel H, 29
Thioredoxin, 42, 187, 326, 382, 390–391
Thylakoid
apoproteins, 8–9, 11–12
biogenesis, 213–226
membrane, 7, 9, 11, 12, 32, 40, 63, 69–73,
148, 159, 172, 174, 175, 177–180,
189, 191, 192, 205, 208, 214, 222,
224, 232, 238, 239, 241, 254, 326,
352, 353, 356, 357, 367, 368, 373,
382, 383, 386, 400–406
Tobacco, 42, 44, 45, 59, 67, 72, 102, 113, 121,
122, 127–134, 161, 163, 177, 197, 246,
250–253, 255, 257, 263, 265–267, 269,
271–279, 285–303, 309, 310, 316, 320,
352, 354, 382, 386, 388, 389, 407, 408
BY-2 cells, 127–134
plastome, 251, 287–290, 302, 303
Tocochromanols, 155–166
Tocopherol, 121, 122, 155–166, 383–388, 402
level of, 112, 158
localisation, 96
Tocotrienol, 155–166
Transformation, 64, 251–254, 256, 257, 264,
267–275, 278–280, 287, 290, 292, 300,
302, 303, 309, 313, 314, 316, 320, 354,
374, 407
Transgene, 123, 252, 253, 257, 263, 264, 267–275,
279, 289, 291, 293, 314
cassette, 267, 269, 270
containment, 253, 257, 263, 267, 275
Transition dipoles, 12
Translation efficiency, 254, 298
Transmembrane electron transport, 370
Transplastomic, 251–257, 270–272, 274, 279,
280, 288, 290-296, 298
Trigalactosyldiacylglycerol (TGDG), 196, 205
Tropospheric ozone, 324, 325, 327, 331
Tyrosine, 62, 157, 160, 163, 289, 334
U
Ubiquinone, 96, 101, 102, 120, 128
biosynthesis, 101, 102, 120
localisation, 96
UDP-sulfoquinovose (UDP-SQ), 175, 176, 179
Unfolded state, 8–10, 20
Uridine-diphosphate-galactose (UDP-Gal),
186–188, 192, 193, 205, 208
Uroporphyrin III, 408
V
Vaccine antigens, 263–265, 269, 272, 273,
275–277
4VChlR. See 4-Vinyl Chl a reductase
4VCR. See 4-Vinyl chlorophyllide a reductase
4-Vinyl Chl a reductase (4VChlR), 8, 28, 35
4-Vinyl chlorophyllide a reductase (4VCR), 8,
28–36
Vinyl groups, 27, 58
[4Vinyl] Mg-protoporphyrin monoester reductase
(4VMpeR), 29–31, 34–37
[4-Vinyl] Mg-proto reductase (4VMPR), 8,
28–31, 35
4-Vinyl Pchlide a reductase (4VPideR),
8, 27–36
[4-vinyl] reductase (4VR), 8, 26–35
Violaxanthin, 232, 350, 384, 387, 402
Violaxanthin de-epoxidase, 350, 384, 387
Vitamin B3, 33
Vitamin B6, 402, 407
Vitamin E, 112, 114, 155–166
Vitamin K, 4, 112, 165
422
Page 453
Subject Index
(4VMpeR). See [4Vinyl] Mg-protoporphyrin
monoester reductase
4VMPR. See [4-Vinyl] Mg-proto reductase
4VPideR. See 4-Vinyl Pchlide a reductase
4V-Proto, 34
4VR isoforms, 28
W
Walker B motif, 41, 80, 81
Water soluble chlorophyll
binding proteins, 402
Water water cycle, 348, 349, 351–352,
356, 391, 392
Wave number, 16–17
Wild watermelon, 363–374
X
Xantha−F, 43, 79, 80, 85
Xantha−H gene, 80
Xanthophyll cycle, 60, 112, 207, 350, 387
Xanthophylls, 220, 222, 386, 387, 402
Xerophytes, 363–374
Z
Zeaxanthin, 112, 207, 350, 384, 387, 399, 402
423
