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Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998. 49:525–55
Copyright
c
°
1998 by Annual Reviews. All rights reserved
EVOLUTION OF LIGHT-REGULATED
PLANT PROMOTERS
Gerardo Arg
¨
uello-Astorga and Luis Herrera-Estrella
Departamento de Ingenier´ıa Gen´etica de Plantas, Centro de Investigaci´on y de Estudios
Avanzados del IPN, Apartado Postal 629, 36500 Irapuato, Guanajuato, M´exico
KEY WORDS: gene evolution, plant evolution, plastid-nuclear interactions, photoreceptors
ABSTRACT
In this review, we address the phylogenetic and structural relationships between
light-responsive promoter regions from a range of plant genes, that could explain
boththeircommondependenceonspecificphotoreceptor-associatedtransduction
pathways and their functional versatility. The well-known multipartite light-
responsive elements (LREs) of flowering plants share sequences very similar to
motifs in the promoters of orthologous genes from conifers, ferns, and mosses,
whose genes are expressed in absence of light. Therefore, composite LREs have
apparentlyevolvedfromcis-regulatoryunitsinvolvedinotherpromoterfunctions,
a notion with significant implications to our understanding of the structural and
functional organization of angiosperm LREs.
CONTENTS
INTRODUCTION ........................................................... 526
LIGHT REGULATION OF GENE TRANSCRIPTION: A BRIEF OVERVIEW ..........527
Control of Gene Expression by Photoreceptors .................................527
Light-Responsive Promoters ................................................527
The Phylogenetic-Structural Sequence Analysis ................................. 528
EVOLUTION OF LREs IN Lhcb PROMOTERS................................... 529
The Proximal LRE of Lhcb 1 Genes ..........................................529
Evolution of the Proximal Region of Lhcb1 Promoters............................ 531
LREs in the Central Region of Lhcb1 Promoters ................................532
Evolution of the Central LRE of Lhcb1 Promoters ............................... 532
Delimitation of a LRE in Lhcb2 Promoters ..................................... 533
Evolution of Lhcb2 Promoters ............................................... 533
EVOLUTION OF LREs IN rbcS PROMOTERS ................................... 534
The Light-Responsive Box II-III Region .......................................534
Evolution of the Box II-III Homologous Regions ................................536
525
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The Light-Responsive I-G Unit .............................................. 538
Evolution of the I-G Region .................................................538
EVOLUTION OF THE LIGHT-REPRESSED PHYTOCHROME A PROMOTER ........539
Functional Organization of phyA Promoters ................................... 539
Evolution of phyA Promoters................................................ 539
Evolution of chs Promoters ................................................. 540
EVOLUTION OF LIGHT-REGULATED PARALOGOUS GENE PROMOTERS .........542
Differential Activity of Paralogous Gene Promoters.............................. 542
Do Paralogous Promoters Evolve by Nonrandom Processes? ......................543
LRE-ASSOCIATED CMAs ....................................................544
CMAs in Additional Plant Genes ............................................544
Structural Analogies Between LRE-Associated CMAs ............................ 544
Common Structural Features of Composite LREs................................ 545
Evolution of LREs: The Chloroplast Connection ................................ 546
CONCLUDING REMARKS ...................................................549
INTRODUCTION
Photosynthesis is an ancient biochemical process that probably evolved 3500
million years ago (111). The nuclear genome of higher plants encodes proteins
homologous to cyanobacterial proteins of photosynthesis; because these bac-
teria are the living descendants of the original photosynthetic organisms, plant
genes encoding such proteins are among the oldest genes of eukaryotes.
To date, molecular evolution studies have concentrated on the coding se-
quences of gene families. The evolution of regulatory sequences, which de-
termine where, when, and the level at which genes are transcribed, has been
largely neglected. In the case of the photosynthesis-associated nuclear genes
(PhANGs) from higher plants, interesting evolutionary aspects of the molec-
ular mechanisms by which transcription is activated by light receptors (e.g.
phytochrome) could be addressed through the comparative analysis of pro-
moter sequences. For instance, why does light profoundly affect transcription
of PhANGs in monocotyledonous and dicotyledonous plants, while PhANG
promoters in conifers, ferns, and mosses are either light insensitive or, at most,
weakly photoresponsive (4,71, 89,99, 129). The systematic comparisons of
angiosperm and nonflowering plant PhANGs promoter sequences provide a
unique opportunity to explore how a new regulatory function, light respon-
siveness, was incorporated into the promoters of a wide range of genes whose
expression is coordinately regulated.
Besidesitsobviousrelevanceforevolutionarystudies, acomparativeanalysis
of the structure of photoregulated promoters can be useful to address other
important issues in plant gene expression. Comparative analysis of PhANG
upstream sequences may contribute to reduce the apparent diversity of light-
responsive elements(LREs)by revealingconcealedphylogenetic and structural
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PROMOTER EVOLUTION 527
relationships between dissimilar promoter regions with analogous functions.
Other important issues concerning the composition and functional organization
of LREs in plant genes could also be uncovered by their analysis from an
evolutionary perspective.
The purpose of this review is to address the phylogenetic and structural
relationships between light-responsive promoter regions from orthologous and
paralogous plant genes. We review LREs from a wide range of genes, explore
theircommondependenceon specificphototransduction pathways,and analyze
correlations between the composition of multipartite LREs and their overall
functional properties.
LIGHT REGULATION OF GENE TRANSCRIPTION:
A BRIEF OVERVIEW
Control of Gene Expression by Photoreceptors
The responses of plants to light are complex: seed germination, de-etiolation of
seedlings, chloroplast development, stem growth, pigment biosynthesis, flow-
ering, and senescence (67). Most of these responses require changes in both
chloroplast and nuclear gene expression, which are mediated by three major
classesofphotoreceptors: phytochromes, blue/UV-Alight receptors, andUV-B
light receptor(s) (2,61,100). Light-regulated genes may respond to more than
onephotoreceptor, thus allowinga finely tuned control of their expressionwhen
stimulated by light (123).
The best characterized light receptor is phytochrome (PHY), which exists in
two photochemically interconvertible forms, Pr and Pfr, and is encoded by a
small family of genes in angiosperms (42,99, 100). PHY controls the expres-
sionofdiversegenesatthe transcriptional, posttranscriptional, andtranslational
levels (43,112,123). Gene expression is regulated by at least three different
signal transduction pathways activated by PHY: one depends on cyclic GMP
(cGMP), which regulates genes such as those involved in anthocyanin biosyn-
thesis in some species; a second pathway depends on calcium/calmodulin,
which activates a subset of chloroplast-associated nuclear genes (17, 85); and a
third signal pathway, whichrequires both calcium and cGMP, activates a subset
of genes necessary for chloroplast development (e.g. the gene encoding ferre-
doxin NADP+ oxidoreductase) (18), and represses transcription of phy-A and
the gene encoding asparagine synthetase (91).
Light-Responsive Promoters
In flowering plants, light regulation of nuclear genes occurs mainly at the tran-
scriptional level, as demonstrated by nuclear run-on transcription assays and
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promoter-reporter gene fusions (112,122,126). The most extensively studied
light-responsive genes are those encoding the small subunit of ribulose-1,5-
bisphosphate carboxylase/oxygenase (rbcS) and the chlorophyll a/b binding
proteins (Lhc, formerly called Cab), both of which are a paradigmfor PhANGs
controlled by the calcium/calmodulin phototransduction pathway (17). Chal-
cone synthase (chs) genes, on the other hand, have been the model for genes
involvedinthe anthocyaninbiosyntheticpathway insome dicots and, hence, for
genestargetedbythephytochromesignalpathwaydependentoncGMP(17,85).
More recently, PHY-A genes have become a model for the diverse genes whose
transcription is down-regulated by light and which are controlled by the third
phytochrome signaling pathway, dependent on calcium and cGMP (91).
A plethora of cis-acting elements and protein factors presumably involved
in transcriptional light responses have been identified (13,16, 122,126); how-
ever, conclusive evidence for an essential role in light responsiveness has been
obtained for only a few of them (5,41, 66,136). Several general conclusions
are possible: 1. No single conserved sequence element is found in all light-
responsive promoters. 2. The smallest native promoter sequences, sufficient to
confer light inducibility on heterologous minimal promoters, are multipartite
regulatoryelementsthatcontaindifferentcombinationsofcis-actingsequences.
3. Even the smallest known photoresponsive promoter regions, when exam-
inedina heterologouscontext, displayfairlycomplexresponses, oftenretaining
the dependence on light wavelength, developmental stage of chloroplasts, and
tissue specificity of the native promoter. 4. Numerous protein factors bind
sequences within photoregulated promoters, although their actual contribution
to light-activated transcription remains uncertain (13,122,126,128).
The Phylogenetic-Structural Sequence Analysis
A commonly used approach to identify regulatory cis-elements is to search for
conserved DNA motifs within the promoter region of orthologous genes. Such
analyses have been successful in identifying cis-acting elements involved in
the light responsiveness of PhANGs, such as the G-box and I-box elements
from rbcS genes (48) and the GATA motifs of Lhcb1 genes (44). However,
regulatory elements showing sequence degeneracy are not easily recognized in
comparative analyses.
Sequence heterogeneity of regulatory elements may be functionally over-
come if multiprotein regulatorycomplexes facilitatebinding to imperfect target
sites (86,135). Because conventional computer programs for DNA sequence
comparisons can fail to detect evolutionarily related but structurally variable
promoter regions with analogous functions, alternative approaches have been
developed, such as the “phylogenetic-structural method” of sequence analy-
sis (8,10). This method is based on the search of “homologous” (rather than
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PROMOTER EVOLUTION 529
“similar”) DNA sequences of a functionally characterized promoter. Two se-
quences are homologous when they share common ancestry, regardless of the
degree of similarity between them (37). In this sense, the G-box elements of
rbcS, chs, and Lhcb1 genes are not homologous but only similar because they
have different evolutionary origins, whereas the rbcS I-G unit of solanaceous
species is probably homologous to the rbcS X-Y promoter region of Lemna,
an aquatic monocotyledonous plant, despite their rather low overall sequence
similarities (10).
The individual elements found within a multipartite cis-regulatory region
are termed phylogenetic footprints (PFs); they share high conservation over
a segment of 6 contiguous base pairs in alignments of orthologous upstream
sequences and represent potential binding sites for transcription factors (53).
A cluster of PFs whose arrangement (combination, spacing, and relative ori-
entation) is conserved through a phylogenetic series of homologous promoter
regions is termed a conserved modular arrangement (CMA). If a given CMA
consistently correlates with experimentally defined light-responsive promoter
regions, then it is called an LRE-associated CMA. In this method, sequence
comparisons are made in a phylogenetically ordered fashion, because the over-
all structure of multipartite regulatory units tends to diverge in evolution. Thus,
homologous genes from species belonging to the same plant taxon should be
compared first. Comparisons with other taxons follow. This procedure allows
us to discern how an ancestral multipartite regulatory module has changed in
an evolutionary context and can establish phylogenetic relationships between
promoter regions that are apparently unrelated by structural criteria. An exam-
ple of this analysis applied to Lhcb1 light-responsive regions is presented in
Figure 1a.
EVOLUTION OF LREs IN Lhcb PROMOTERS
The Proximal LRE of Lhcb 1 Genes
Three types of chlorophyll a/bbinding proteins are found in the major light-
harvesting complex of photosystem II, encoded by Lhcb1, Lhcb2, and Lhcb3
(52,60). Most Lhcb promoters that have been functionally analyzed are from
theLhcb1 gene familyand typically lackintrons. In Lhcb1genesfrom dicotyle-
dons, an LRE is located in the proximal promoter region of these genes. This
LRE is characterized by three conserved GATA motifs spaced by 2 and 6 bp,
respectively, which are located between the CCAAT and TATA boxes (44,87).
In Arabidopsis Lhcb1
∗
1 (formerly Cab2), the −111 to −33 region is sufficient
to confer a pattern of expression dependent on both PHY and a circadian clock,
to a heterologous minimal promoter (6). A nuclear factor that specifically inter-
acts with the triple GATA repeats found in this LRE was identified and named
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CGF-1 (6). If the three GATA motifs are altered by site-directed mutagenesis,
the interaction of CGF-1 is disrupted and responsiveness to PHY and part of
the light-induced circadian oscillation of Cab2 expression are comprised (5).
Mutational analysis of the Arabidopsis Lhcb1
∗
3 (Cab1) gene promoter iden-
tified additional cis-acting motifs, that could be involved in the functionality
of this LRE. Mutations in a 27-bp region upstream the CCAAT box, which
is bound by the CA-1 factor (75a), drastically reduced the overall promoter
activity and also eliminated PHY responsiveness (68). More recently, a Myb-
related transcription factor that specifically interacts with a conservedsequence
motif [AA(C/A)AAATCT] within the CA-1 region was cloned (131). Trans-
genicArabidopsisexpressinganantisensemRNAfor thisfactor(calledCCA-1)
showed reduced PHY induction of the endogenous Lhcb1
∗
3 gene, whereas ex-
pression of other PHY-regulated genes, such as rbcS, was not affected; thus
CCA-1 has a specific role in Lhcb1 photoregulation (131).
Evolution of the Proximal Region of Lhcb1 Promoters
At least five PFs are found within the first 110–130 bp of the Lhcb1 promoter
sequences from dicotyledons. All these PFs bind defined proteins. The most
distal PF is the CUF-1 binding site, a G-box-related sequence which functions
as a general activating element (6). The second PF is the CCA-1 binding
site (131). The third is the CCAAT-box, which is part of the binding site of
Tac, a protein factor proposed to be involved in the regulation of Arabidopsis
cab2 by the circadian clock (22). The fourth and fifth PFs are located in the
CGF-1 binding region, comprising the three GATA motifs located upstream to
the TATA box. Comparative analyses indicate that these GATA elements are
distinct from both the phylogenetic and the structural point of view. 1. GATA I
is part of a PF whose consensus is GATAAGR (the I-box motif) (48), whereas
GATA II/IIIformasinglePFwithaGATANNGATAconsensusindicotyledons.
2. Apparently GATA I is a more ancient element than GATA II/III, inferred
from the fact that the former, but not the latter, element is present in Lhcb
promoters of gymnosperms (11,71).
←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Figure 1 (a) Lhcb1 promoter regions that are homologous but dissimilar. The indicated CGF-1
binding site was defined by Teakle & Kay (121). The Z-DNA element of the Arabidopsis Lhcb1
∗
3
promoter has been functionally characterized by Ha & An (54) and by Puente et al (98). The
illustratedregion correspondsto thecabCMA3 ofthegenes indicatedin thefigure. (b)Hypothetical
arrangement of the upstream LRE of Lhcb1 promoters in the common ancestor of Dicotyledons.
Twoputative LREs derived from the ancestor, which have been previouslyidentified as cabCMA-3
and cabCMA-2 (10), are shown. GATA-containing sequences of maize genes that are inverted with
respect to dicot homologous motifs are underlined. Notice that in some cases, a CCA-1 motif is
the evolutionary counterpart of an I-box element.
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Within dicots only the CCAAT and GATA motifs are invariably present in
the TATA-proximal region. The CUF-1 and CCA-1 binding sites are found
in some but not all Lhcb1 genes. Only one tomato gene (Lhcb1
∗
5) contains
both CUF-1 and CCA-1 binding sites, four (Lhcb1
∗
1,
∗
2,
∗
3, and
∗
4) contain
the CUF-1 element but lack the CCA-1 site, and two (Lhcb1
∗
6 and
∗
7) lack a
discernible CUF-1 site but contain an inverted CCA-1 binding site. Although
it is probable that these structural differences determine qualitative differences
in the regulation of these paralogous promoters, transcript abundance in tomato
leaves is not correlated with the composition of their proximal region (97).
Most of the known Lhcb1 genes of monocotyledons have promoters clearly
distinct from those of dicots, with two exceptions: the Lemna Lhcb1
∗
1 (AB30)
and the maize Lhcb1
∗
2 (cab-1) genes (69,118), both containing a (CUF-1
site)-(CCAAT-box)-(GATAII)-(I-box)arrangementhomologoustothatofdicot
promoters (10). This arrangement in Lhcb1 promoters may either predate the
divergenceofmonocotsand dicotsorresultfromconvergentevolution. Support
for an ancient origin comes from an orthologous gene of a conifer (Pinus
contorta) that has a promoter (CCAAT-box)-(I-box)-(TATA-box) arrangement
that is similar to that found in angiosperms (see Figure 6). The pine gene lacks
the GATA III, CCA-1, and CUF-1 elements, suggesting that these elements
probablyevolvedafter thedivergenceof thelineages leadingto modernconifers
and angiosperms.
LREs in the Central Region of Lhcb1 Promoters
Lhcb1 genes contain additional LREs, besides those found in the TATA-proxi-
malregion. Castresanaetal(23)demonstratedbygain-of-functionexperiments
the photoresponsiveness of the −396 to −186 region of the tobacco Cab-E
gene. A light-responsive region has also been mapped to the −347 to −100
promoter region of the pea Lhcb1
∗
2 (AB80) gene. This 247-bp fragment was
shown to function as a light-responsive, tissue-specific enhancer in gain-of-
function experiments (113). Two nuclear factors binding this regulatory region
were identified, one of which (ABF-1) is found only in green tissues (7). By
systematic deletion the AB80 enhancer light-responsive core is located in the
−200 to −100 region (Arg¨uello-Astorga & Herrera-Estrella, manuscript in
preparation). EvidenceforLREsinthe−240 to−100 regionoftheArabidopsis
Cab2 promoter has been also reported (121).
Evolution of the Central LRE of Lhcb1 Promoters
The comparative analysis of the tobacco CabE and pea AB80 upstream LREs,
with the corresponding promoter segments from other Lhcb1 genes from di-
cots, suggests a structure of this promoter region in the common ancestor of
dicotyledons. An extensive ancestral CMA encompassing at least five PFs is
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PROMOTER EVOLUTION 533
inferred (Figure 1b). This ancestral organization is still conserved in some
genes of leguminous species [e.g. pea Cab-8 (3)]. The central PF of this CMA
is a sequence similar, but not identical, to the G-box from rbcS genes. In to-
bacco CabE this G box–like element (G
∗
box) is associated with a Box II–like
element corresponding to a PF with a GATA core motif (23). Homologous G
box–like and 5
0
associated GATA-motif elements (I
∗
box) exist in members of
the Lhcb1 gene family in plants belonging to four orders of dicotyledons. A
third PF (YCCACART) is found immediately upstream of the G-box element
in several Lhcb1 genes of legumes and the tobacco Cab-E promoter but not
in other dicot genes. Interestingly, this PF is also found in the homologous
region of two maize Lhcb1 genes (Figure 1b), suggesting a very ancient origin
of this PF. A fourth PF with the consensus CATTGGCTA closely precedes a
PF encompassing an I-box motif located 15–20 bp downstream of the G-box
element. The arrangement of this Lhcb1 region (cabCMA2) is highly analo-
gous to that of the G-, I-box region of dicot rbcS promoters, with a very similar
PF associated 5
0
to the I-box motif. The resemblance in some cases is so strik-
ing that a Lhcb1 promoter (e.g. pea AB80) can display more similarity in this
region with the analogous rbcS promoter segment (e.g. pea rbcS 3A) than with
certain homologous Lhcb1 regions (10). The analogies between the overall
structural organization of the I
∗
-G
∗
-I promoter region of Lhcb1 genes and the
I-G-I unit of rbcS promoters are intriguing and suggest either a common ances-
try or convergent evolution of these regulatory promoter modules.
Delimitation of a LRE in Lhcb2 Promoters
Although comparatively few members of the Lhcb2 gene family have been
studied, the promoter of one, the Lhcb2
∗
1 (formerly AB19) gene from Lemna
gibba,hasbeencharacterizedingreatdetail. Deletionanalysis, linkerscanning,
and site-directed mutagenesis identified two 10-bp elements in the −134 to
−105 region that are critical for light responsiveness. One of them contains
the I box–related GATAGGG motif and the other a CCAAT motif. Mutation
of the latter element led to high levels of expression in the dark, suggesting
that it binds a repressor in the absence of light. Mutations in the I-box motif
led to complete loss of red-light responsiveness, suggesting that this region is
involved in PHY- mediated light activation of transcription (66). More detailed
site-directed mutagenesis of those 10-bp regions allowed the identification of
two shorter sequences (REα = AACCAA and REβ = CGGATA) that are
critical for AB19 light regulation (31).
Evolution of Lhcb2 Promoters
Genomic clones of Lhcb2 genes have been isolated from the moss Physcomi-
trella patens (79), the fern Polystichum munitum (96), the conifer Pinus
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thunbergii(71), themonocotLemnagibba(64),andthreedicotyledonousplants
(pea, Petunia, and cotton) (39,103,115). These promoters contain a number of
PFs, two of which correspond to the Lemna REα and REβ elements (Figure 2).
Only a few of the identified PFs are present in all species. Among the PFs
common to most if not all the known Lhcb2 promoters are the Lemna REα ele-
ment,generallyrecognizedasaconservedCCAATbox, andaG(G/A)AAATCT
motif, which is similar to the CCA-1 binding site of the Lhcb1 genes.
An interesting observation is that the gene harboring sequences with the
highest similarity to the Lemna REα and REβ light-responsive elements is
that of P. thunbergii (see Figure 2), whose promoter directs light-independent
gene expression in both its native context (71) and in transgenic angiosperms
(70,138). This paradoxical observation is discussed below. Another relevant
observation is that Lhcb2 genes from dicotyledons lack a REβ element, instead
displaying three lineage-specific PFs, two of which include inverted GATA
motifs (Figure 2). It would be interesting to determine whether those elements
are functionally equivalent to REβ.
Upstream sequences of Lhcb2 and Lhcb1 genes are probably derived from
a common ancestral promoter, because they display a similar overall struc-
turalorganization, witha(GBox/CUF-1site)-(CCA-1element)-(CCAAT-box)-
(I-box)-(TATA box) basic arrangement. Spacing between these elements is,
however, very different in the two gene families.
EVOLUTION OF LREs IN rbcS PROMOTERS
The Light-Responsive Box II-III Region
The pea rbcS-3A gene has been used as a paradigm for the study of light-
regulated gene expression in dicotyledons. Analysis of the rbcS-3A promoter
has uncovered three independent regions that contain an LRE (47). The LRE
located in the −166 to −50 region has been characterized in most detail (45).
This region includes two elements called Box II and Box III, both of which are
binding sites for a nuclear factor named GT-1 (49). This factor binds in vitro to
sequences related to the degenerate consensus (A/T) GTGPu (T/A) AA (T/A)
(50). A synthetic tetramer of the pea Box II element (GTGTGGTTAATAATG)
conferred light-responsive transcriptional activity to the −90 CaMV 35S pro-
moter (75,98) but was unable to enhance transcription when fused to either
the −46 CaMV 35S or the −50 rbcS-3A minimal promoters (28). This ele-
ment appears necessary, but not sufficient, for light-regulated transcriptional
activation. Arabidopsis and tobacco cDNAs encoding GT-1, a Box II DNA
binding proteins, have been cloned and partially characterized (46,58, 95). In-
terestingly, GT-1 is closely related to the GATA-binding nuclear factors CGF-1
and IBF-2b and can bind to similar cognate DNA sequences (121). Two other
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PROMOTER EVOLUTION 535
Figure 2 Sequence changes in Lhcb2 gene promoters from land plants. DNA motifs represented by identical symbols but shaded differently indicate
related but not identical sequences.
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proteins called 3AF-3 and 3AF-5 probably act together with GT-1 to confer
rbcS-3A light-regulated expression; they bind inverted GATA motifs located
at each end of Box III. Mutations in these GATA sequences severely reduced
promoter activity (104).
Evolution of the Box II-III Homologous Regions
Upstream sequences of many angiosperm rbcS genes are known. However,
only two rbcS promoters are known from nonflowering plants, the conifer
Larix laricina (59) and the homosporous fern Pteris vittata (56). Comparison
of the Pteris and Larix proximal promoter regions (−130/−1) reveals only
four PFs, two of which are inverted I box–related motifs: one overlapping
the putative TATA-box of the Larix gene, and the second, with the sequence
GTTATCC, found ∼70 bp upstream. In the Larix promoter, this PF is found
as an imperfect direct repeat, flanked by two additional PFs, one of which
encompasses a CCAAT motif. The relative position of this CMA in the conifer
promoter (i.e. ∼25 bp downstream to the I-box element) is practically identical
tothat of the Box II–3AF3 regionin dicot rbcS promoters. Comparison of these
CMAs uncovers several interesting characteristics:
1. The Box II element seems to be evolutionarily derived from two separate
Pteris/Larix PFs (Figure 3). One of them is the most 5
0
GTTATCC motif
in Larix, which is homologous to the 3
0
half of Box II. This relationship
is especially clear in rbcS promoters of the Brassicaceae (see Figure 6).
Therefore, Box II could be a composite element bound in vivo by two pro-
tein factors, one of them being a GATA-binding factor.
2. The second repeat of the GTTATCC motif of Larix is homologous to a con-
served sequence immediately downstream to Box II, which in Arabidopsis
and Brassica genes is almost identical to the so-called LAMP binding site
(51), an inverted I-box element. In nonbrassicaceous dicots the sequences
immediately downstream of Box II do not resemble the LAMP motif or the
Pteris/Larix PF, but their structural relationship is easily recognizable in a
phylogenetic series (not shown, but see 82).
3. The Pteris/Larix CCAAT-box is apparently homologous to the pea 3AF3
binding site (104). In the conifer promoter the LAMP-like motif and the
CCAAT box are close, but in dicots the 3AF3 element is separated from
the LAMP-related motif by 10–24 bp. Sequences in this intermediate DNA
are functionally relevant, encompassing in pea rbcS-3A the Box III and the
3AF5 elements (104) (Figure 3).
The Box II–containing CMA is absent in all known rbcS genes of mono-
cotyledons (∼10), and in the orthologous genes of a dicot species, the common
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Figure 3 Sequences of rbcS gene promoters in vascular plants.
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ice plant (Azoideae) (35). Our interpretation is that these groups have lost Box
II, which we consider an ancestral feature of rbcS genes.
The Light-Responsive I-G Unit
rbcS promoters usually contain two closely associated elements, the I and G
boxes. Mutations of either the G-box or the two flanking I-box elements of
the Arabidopsis rbcS-1A promoter almost abolished its activity (36). A simi-
lar drastic drop of transcriptional activity was observed in the spinach rbcS-1
promoter when the G-box element was mutated (80). In spite of its functional
relevance in dicots, deletion of a G-box in the rbcSZm1 gene of maize had no
significant effects on promoter activity. Deletion of the associated I-box motif
reduced expression in light 2.5-fold (106).
Lemna rbcS promoters lack a typical G-box element but contain a canonical
I-boxmotifwithin the so-called X-box element, which ispartofthebindingsite
of LRF-1, a light-regulated nuclear factor (21). This I-box motif is included in
a 30-bp region of the Lemna rbcS SSU5B promoter necessary for PHY regula-
tion (31).
Gain-of-function experiments showed that the region of the rbcS promoters
encompassing the I- and G-box elements functions as a composite LRE,able to
direct a tissue-specific pattern of expression almost identical to the native rbcS
promoter, including the dependence on the developmental stage of plastids (9).
Mutation of either the I-box or the G-box eliminated detectable transcription
(9). The I-G region functions as a complex regulatory unit, similar to that of
the light-responsive Unit 1 of the parsley chs gene (108).
Evolution of the I-G Region
The two I-box elements of the I-G-I CMA display a different sequence con-
sensus and are flanked by different conserved sequence motifs. The more
upstream I-box has the consensus GATAAGAT (A/T) and is adjacent 3
0
to a
PF with the consensus (A/T) ARGATGA; the second I-box has the consensus
ATGATAAGG and is 5
0
flanked by a PF with the consensus TGGTGGCTA
(Figure 3). The I-box-associated PFs are conserved in genes of plants belong-
ing to fiveorders of dicotyledons. A homologous I-G-I arrangement is found in
some maize rbcS genes but not in other genes from monocotyledons. However,
CMAs that are probably derived from an ancestral I-G-I structure are present
in all these promoters (Figure 3).
Thefindingthat theI-G (-I)arrangement isalsofoundinthe homologouspro-
moters of a conifer and a fern (Figure 3) is unexpected because these promoters
are presumably light-insensitive, whereas the I-G unit is apparently involved
in responses to light signals in angiosperms. Based on the persistence of the
I-G-I arrangement since at least the divergence of ferns and seed plants, 395
mya (116), we propose that it has played, and probably still does, one or several
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PROMOTER EVOLUTION 539
important functional roles, different to light-regulation, in the control of rbcS
gene transcription.
EVOLUTION OF THE LIGHT-REPRESSED
PHYTOCHROME A PROMOTER
Functional Organization of phyA Promoters
Phytochrome (PHY) is encoded by small gene families in angiosperms; in
Arabidopsis the PHY apoprotein is encoded by five genes (99). Each PHY is
proposedtohaveadifferentphysiologicalrole(100). PHYshavebeenclassified
into two types. The type I, or “etiolated-tissue” PHY, is most abundant in dark-
grown plants, and its Pfr form is rapidly degraded in light by an ubiquitin-
mediated proteolytic process. Type II or “green-tissue” PHY are present in
much lower levels, but their Pfr form is stable in light (99, 100). The only
known type I PHY is that encoded by the phyA gene, whose mRNA abundance
also decreases in light. This inhibition of phyA gene activity is autoregulatory
(PHY-dependent) and operates at the transcriptional level (19,65,77).
The phyA promoters of two monocotyledons, oat and rice, have been func-
tionally characterized. A combination of deletion analysis and linker-scan mu-
tagenesisidentifiedinoatthreecis-regulatoryelementsdesignatedPE1(positive
element-1), PE3 (positive element-3), and RE1 (repressor element-1) (19,20).
PE1 and PE3 act synergistically to support maximal expression under dere-
pressed conditions (i.e. low Pfr levels); mutation of either element decreases
expression to basal levels. In contrast, mutation of the RE1 element results in
maximal transcription under all conditions, suggesting that Pfr represses phyA
transcription through this negatively acting element (19).
Therice phyApromoter hasno elementsimilarto PE1. Instead, thispromoter
contains a triplet of GT-elements that have been shown, in transient expression
assays, to be functionally equivalent to the oat PE1 element (32,99). These
elements, related in sequence to the GT-1 binding sites of rbcS promoters (65),
are bound by a transcription factor, named GT-2 (32,34).
In addition to phyA, several other genes are down-regulated by light (88,92,
123), including the genes encoding asparagine synthetase (127). Recently a
17-bp element was identified that is both necessary and sufficient for the PHY-
mediatedrepressionofthepeaasparaginesynthetasegene.Thissequenceisvery
similar to the phyA RE1 element and is the target for a highly conserved PHY-
generatedrepressor,whoseactivityisregulatedbybothcalciumandcGMP(91).
Evolution of phyA Promoters
Phytochrome genes havebeen found in phototropic eukaryotic organisms rang-
ing from algae to angiosperms (42,99), and genomic clones of phy genes have
been isolated from angiosperms and several lower plants. The latter include
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speciesrepresentativeoflineagesdatedto theSilurian andDevonian, andwhich
diverged more than 400 million years ago (27,110,116).
The cereal PE3-RE1 region is conserved in the phyA promoters of plant
species belonging to three different orders of dicotyledons (1,33, 105), but
no obvious counterpart of the monocot GT-boxes region was detected. The
conservation of the PE3-RE1 arrangement in dicots suggests a conserved reg-
ulatory activity of these elements (33). The phyA upstream sequences of bryo-
phytes(the mosses PhyscomitrellaandCeratodon; 107, 124), alycopodiophyta
(Selaginella; 57), and a psilotophyta (Psilotum; 107) contain a number of PFs.
Two clusters of these PFs or CMAs are common to all reported lower plant
phyA promoters (Figure 4). The CMA nearest the start codon of the mosses
and lower vascular plant genes includes sequences similar to the PE3 core ele-
ment and other flanking sequence elements. The central, most conserved DNA
motif of the lower plant CMA is nearly identical to a sequence element in the
Arabidopsis PE3–RE1 region, immediately upstream of the RE1 motif. No
canonical RE1 element is found in lower plant phy promoters.
Interestingly, the second, more distal lower plant phyA-CMA seems to be the
evolutionary counterpart of the region encompassing the GT boxes in monocot
phyA promoters (Figure 4). Thus, the cis-regulatory elements of monocotyle-
donphyA genesseem tohave evolvedfromcis-acting sequencesalreadypresent
in orthologous genes of the common ancestor of land plants. What the regula-
tory function was of such elements in the primitive land plants is an intriguing
question that could be partially solved by the functional characterization of the
identified phyACMAs in mosses and vascular cryptogams.
Evolution of chs Promoters
In some species, induction of chs gene expression by light is required for
flavonoid accumulation, which provides a protective shield against potentially
harmful UV irradiation (55).
The promoters of parsley and mustard chs genes have been functionally an-
alyzed, and a 50-bp light-responsive conserved region, named light-regulatory
unit1(LRU1),hasbeenstudiedingreat detail(41,62,63). LRU1is sufficientto
confer light- responsiveness to heterologous minimal promoters (63,102,132)
and consists of at least two distinct cis-acting elements, ACEchs and MREchs
(formerly Box II and Box I, respectively) (108,109). ACEchs contains a G-
box element that interacts in vivo and in vitro with bZIP regulatory factors
(40,132). MREchs was originally identified as a 17-bp in vivo DNA footprint
(109) with a conserved sequence motif called the H-box core (78), which is
recognized by PcMYB1, a Myb-related transcription factor of parsley (41).
Recently, it was shown that chs LRU1 activity is controlled by PHY through
the cGMP-dependent transduction pathway (136). Comparative analysis of
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PROMOTER EVOLUTION 541
Figure 4 Sequences of phyA promoters in land plants.
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orthologous chs promoters showed that LRU1 homologous sequences are pre-
sent only in genes of cereals and brassicaceous plants (10). Homologous genes
of legumes, snapdragon, and carrot contain, in the same relative position as
LRU1, a CMA comprising G-box and H-box elements as in LRU1, but spaced
differently (6–8 bp). Several regulatory functions have been assigned to this
G-H box CMA, including transcriptional activation by p-coumaric acid (78)
and tissue-specific transcription (38). Although this CMA is found within
light-responsive regions of some chs genes (e.g. Anthirrinum chs; 76), there is
no direct evidence of a role in light regulation. Because of both their proximal
position to the TATA box and their PF composition, LRU1 and the G-H CMA
are clearly homologous cis-regulatory regions. Nonetheless, evolutionary di-
vergence of chs genes harboring LRU1 and G-H CMA, respectively, date back
to an era before the divergence of lines that gave rise to monocotyledons and
dicotyledons, as inferredfrom the phylogeneticaldistributionofLRU1(10,26).
EVOLUTION OF LIGHT-REGULATED
PARALOGOUS GENE PROMOTERS
Differential Activity of Paralogous Gene Promoters
Several light-regulated genes such as Lhcb, rbcS, and chs are found in multiple
copies in most genomes. Members of these gene families frequently display
quantitative and/or qualitative differences in expression reflecting in part tran-
scriptional regulation (29a, 30,82, 117,133). Some of these functional differ-
ences correlate with differences in promoter architecture. For example, among
the eight rbcS genes of Petunia, only the two most highly expressed (SSU301
and SS611) contain the I-G-box arrangement (29a). Insertion of an 89-bp frag-
ment of the SSU301 promoter containing the I-G unit into the equivalent region
of the weakly expressed SSU911 gene increased its expression 25-fold (29).
Tomato has five rbcS genes (117). Three have promoters with the I-G unit.
ThemRNAsfrom all fivetomato rbcS genes accumulate to similarlyhighlevels
in leaves and light-grown cotyledons; however, only the genes containing the
I-G unit are coordinately expressed in dark-grown cotyledons, water-stressed
leaves, and developing fruits (12). Interestingly, the spacer DNA sequence
between the I-box and the G-box elements is highly divergent in tomato rbcS
genes but conserved in orthologous genes from other plant species. A fruit-
specific factor (FBF) specifically interacts with the I-G spacer DNA sequence
of the tomato rbcS-3A promoter, which correlates with its reduced activity in
developing tomato fruit (84). The tomato rbcS-2 and tobacco rbcS 8.0 display
a very similar sequence to the pea rbcS-3A I-G spacer element, which is bound
in vitro by GT-1 (50). It is conceivable that these “paralogous gene-specific
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PROMOTER EVOLUTION 543
motifs” modulate environmental or tissue-specific effects on the structurally
invariant I-G regulatory unit.
Do Paralogous Promoters Evolve by Nonrandom Processes?
Paralogous gene promoters often diverge in discrete segments, displaying non-
random patterns of structural variation. For example, in the rbcS family of
Arabidopsis the paralogous 1B, 2B, and 3B gene promoters clearly differ from
that of rbcS-1A by a 60-bp internal deletion. This molecular event juxtaposed
the photoresponsive Box II–LAMP element with downstream conserved mo-
tifs, creating a new combination of cis-regulatory elements. In the rbcS-1B
promoter an additional deletion event removed a 44-bp region encompassing
the I-G-I Unit, juxtaposing the two I boxes originally flanking the G-box se-
quence (72). This gene is the only member of the Arabidopsis rbcS gene family
unable to respond to light pulses (30).
The evolution of discrete, short regulatory elements interspersed along the
promoters of paralogous genes also seems to occur, and this is exemplified by
the maize rbcSZm1 and rbcZm3 genes. Their promoter sequences are very
similar but differ in the presence of small insertions, which are distributed in
a discontinuous pattern (Figure 5a). Some of these paralogous gene-specific
motifs are cis-regulatory elements (106).
Figure 5 Paralogous gene promoters. (a) Schematic comparisons of two maize rbcS promoters
mainlydifferingbysmallinsertion/deletionsevents;somechangescreatecis-actingelements[based
on data from Sch¨affner & Sheen (106)]. (b) Schematic comparison of two functionally distinct
Lhcb1 promoters of pea. Segments of high sequence divergence coinciding with relevant cis-
regulatory elements are shown. Clear rectangles represent blocks of conserved sequences, whose
similarity is indicated as the ratio between the number of identical nucleotides and the overall
longitude (in bp) of the compared promoter segments.
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A probable example of evolution of differential function by loss of specific
cis-acting elements is available with the Lhcb1 genes of pea. Two of these
genes (Cab-8 and AB96) showed significant transcript accumulation after a
red light pulse, whereas the other three Lhcb1 genes (AB80, AB66, and Cab-9)
requirecontinuousredlightforsignificantexpression(133,134).ThepeaCab-8
gene encodes a mature protein 99.5% similar to that of the AB80 and AB66
genes (3, 125) and it displays significant similarity in the 350-bp proximal
part of the promoter. Cab-8 has a consensus dicot Lhcb1 promoter, with a
distal I
∗
-G
∗
-I structural unit and a proximal arrangement of elements (CUF-1)-
(CCA-1)-(CCAAT-box)-(CGF-1 site). In the AB80 and AB66 promoters the
originalCCAATboxsequenceseems tohavebeeneliminated byan 8nt internal
deletion, the CUF-1 binding site is lost by multiple nucleotide substitutions,
and the conserved GATA motif, upstream to the G-box, is mutated in the G
residue and in a few additional upstream nucleotides (Figure 5b). Because the
Cab-8 promoter has the organization of the hypothetical, ancestral dicot Lhcb1
promoter,thearchitectureoftheAB80andAB66promoterscouldbeconsidered
as derived, by mutation and deletion of specific cis-regulatory elements, from
a Cab-8-like promoter. The cause of the mutations and the selective forces that
fixed them in the species remain unknown.
LRE-ASSOCIATED CMAs
CMAs in Additional Plant Genes
Photoresponsiveregionshavebeendefinedinothergenesbydiverseapproaches
(13,122). Some cis-regulatory elements different to those identified in rbcS,
chs, and Lhcb promoters have been proposed for light-regulated transcrip-
tion (14,81, 93). Discrete arrays of sequence motifs in light-responsive re-
gions of those genes are conserved between phylogenetically distant plant
species (10). Some of these LRE-associated CMAs are present in orthologous
genes from both monocots and dicots, indicating a very remote evolutionary
origin. These ancient CMAs are found in genes encoding ferredoxin, and
the pyruvate–orthophosphate dikinase, sedoheptulose-bisphophatase, and the
A subunit of chloroplast glyceraldehyde 3-phosphate dehydrogenase. LRE-
associated CMAs were also identified in dicot genes encoding plastocyanin,
subunits of the chloroplast ATPase, a 10-kDa protein of photosystem II,
4-coumarate:CoA ligase, and phenylammonia-lyase (10).
Structural Analogies Between LRE-Associated CMAs
Mostofthe ∼30identified CMAs(10) canbegroupedinasmallset ofstructural
and phylogenetic types.
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PROMOTER EVOLUTION 545
1. The(I-box)-(G-box)-(I-box)arrangement. IncludedaretheI-GandG-Iunits
of rbcS promoters and their evolutionary variants, including the (X-box)-
(Y-box) regionof Lemna genes(Figure 3); theI
∗
-G
∗
-Iancestral arrangement
of Lhcb1 genes found in legumes, and their evolutionary derivatives such as
the (GATA-motif)-(Z-DNA) region of Arabidopsis Lhcb1
∗
3, the (Box II)-
(G-box) arrangement of tobacco CabE, and the (G-box)-(CCA-1 element)
region of some spinach, tobacco, and Arabidopsis genes (Figure 1); also in
this CMA group are included the I
∗
-G-(I) array of Fed promoters; and the
inverted I-G-I unit of dicot and monocot sbp genes.
2. The (GT-1)-(LAMP-site)-(GT-1) arrangement, observed in both the Box
II-3AF3 region of rbcS genes (rbcS CMA-3) and in the CMA-1 of LS genes
3. The (CCAAT-motif)-(GATA/I-box) combination, found in several light-
responsive promoters, including the REα-REβ unit of Lemna Lhcb2
∗
1 (i.e.
cabCMA4), the (CCAAT)-(GATA I-III) arrangement from Lhcb1 promot-
ers (i.e. cabCMA1), the (CCAAT box)-(motif 15) from solanaceous rbcS
genes (i.e. rbcS CMA-2), and the CMA containing the PC2 region from
plastocyanin gene promoters (i.e. PcCMA-2).
4 The (LAMP-site)-(TATA-box) arrangement, characteristic of all of the sola-
naceous rbcS promoters (82) and found in a modified form in the −50/+15
light-responsive region of pea rbcS-3A (73). This arrangement is also ob-
servedin the LRE-associated CMA of atpC, in plastocyanin gene promoters
(i.e. PcCMA-1), and in gapA CMA-1.
5. The (G-box)-(H-box) arrangement, found in the three identified CMAs of
chs genes, including the photoresponsive units 1 and 2 of parsley chs gene
(108,109).
Common Structural Features of Composite LREs
Do all, or most, of the genes whose transcription is dependent on PHY harbor
a common cis-regulatory element in their promoters? This appealing idea has
not been confirmed by the sequence data from the dozens of PHY-dependent
genes. The identification of LRE-associated CMAs provides a new opportunity
to assess whetherthe regulatory regions of those genes sharestructural features
that could explain their common dependence on such a photoreceptor. The
comparative analysis of ∼30 of these natural combinations of sequence motifs
led to two important findings. 1. All of the LRE-associated CMAs present in
PhANGs include at least one sequence identical, or related, to either the I-box
core motif or its inverted version, the LAMP-site. 2. All of the CMAs found
in genes encoding enzymes involved in the metabolism of phenylpropanoids
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(PhEMAGs) share a conserved module related to the chs H-box core motif,
ACCTA(A/C) C (A/C) (10).
Because PHY regulates expression of its target genes by three different
transduction pathways (85), the superfamily-specific conserved motifs could
be binding sites for transcription factors targeted by specific PHY-signaling
pathways (10). Based on the knowledge of the genes that are activated or re-
pressed by these phototransduction pathways, it has been proposed that the I-
box/GATA-bindingfactorsaredirectorindirecttargetsoftheCa2
+
/calmodulin-
dependent transduction pathway, whereas transcription factors binding at the
H-box motifs in PheMAG CMAs would be affected by the cGMP-dependent
phototransduction pathway (10).
A general model of LRE function proposes that LREs are multipartite cis-
regulatory elements with two general components: “light-specific” elements
and“couplingelements.” Theformerareboundbytranscriptionfactorstargeted
bythelight-signaltransductionpathways(i.e. I-box/GATA-bindingfactors and
HBFs), which confer photoresponsiveness. Coupling elements are bound by
either cell-specific factors or regulatory proteins targeted by other signaling
systems; consequently, the light stimulus to transcription is coupled to other
endogenous and exogenous signals.
Using microinjection into single cells of the tomato aurea mutant, Wu et al
(136) established that constructs containing either 11 copies of the rbcS Box II
element or 4 copies of chs Unit 1 are activated by differentPHY signaling path-
ways. BoxII isaffectedbythe calcium-dependentpathwayand thechsUnit 1is
activated by the cGMP pathway. Taking into account that GT-1, the factor that
binds Box II, is highly related to the nuclear factors CGF-1 and IBF-2b, both
of which bind I-box/GATA motifs (121) the work by Wu et al (136) supports
the hypothesis that factors interacting with I-box-related sequences are targets
for the Ca2+/calmodulin PHY activated pathway. Moreover, Feldbr¨ugge et al
(41) recently determined that the light-responsive core of parsley chs LRU1 is
indeed the H-box, making it the most likely target of the cGMP pathway.
Evolution of LREs: The Chloroplast Connection
The finding that LREs from angiosperm gene promoters are very similar to
putative regulatory units present in promoters from conifers and lower plants
(Figure6)isunexpected, becauseitisgenerallyassumedthatsuchpromotersare
either light insensitive or, at most, weakly photoresponsive. Such physiology is
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 6 Similarities of light-responsive elements of angiosperm with homologous promoter
sequences in nonflowering plants. Notice that Petunia Cab 22R and P. thunbergii Cab-6 belong to
different gene families (i.e. Lhcb1 and Lhcb2, respectively) and that rbcS Box II contains two PFs.
Asterisks denote mismatches between aligned sequences.
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well established in conifers (4,71,89, 94,137), although to our knowledge, no
detailed molecular studies have been carried out in pteridophytas and bryophy-
tas. Conifers and other nonflowering plants (Gingko biloba being an exception;
24, 25) develop chloroplasts when grown in darkness (83,129,130), indicating
that their PhANG promoters are activein the dark. A central question emerges:
did light-responsiveness evolve by changes in cis-regulatory elements or trans-
acting factors, or by both.
BecauseI-box/LAMPelements, which arecritical forPHYresponsivenessin
angiosperms, are also components of ancestral, presumably non-photorespon-
sive, regulatory units of Lhcb and rbcS genes, it is probable that factors bind-
ing these motifs became direct or indirect targets of light-signaling pathways
in organisms preceding flowering plants. This notion is in agreement with
the available experimental evidence, including the recent demonstration that
synthetic pairwise combinations of I-box sequences with diverse conserved el-
ements function as complex LREs (98). However, the presence of an I-box
in combination with other conserved sequence motifs is not necessarily suf-
ficient for light regulation. The Pinus thunbergii cab-6 promoter containing
Reα and Reβ (an I-box motif) elements identical to those of the Lemna AB19
gene (Figure 6) directs a light-independent and tissue-specific expression of a
reporter gene in both dicots and monocots transgenic plants (70,138). There-
fore, other cis-acting signals in addition to the I-box core seem to be necessary
for proper light control in flowering plants.
Ourdata suggest that compositeLREs evolved fromregulatory unitsthatper-
formed functions other than light-regulation. What could these functions have
been? In the case of PhANGs, we hypothesize that these functions were related
to nuclear gene regulation by chloroplast-derived signals. This possibility is
supported by the finding that even the smallest light-responsive PhANG pro-
moter segments display a tissue-specific and chloroplast-dependent pattern of
expression similar to that of entire promoters; to date no evidence has been ob-
tained that these two functions can be separated (9, 14,15, 74,98, 114,120).
Because coordination of gene expression between nuclear and chloroplast
genomes should have evolved a long time before terrestrial plants (101), it
is plausible that PhANG cis-acting promoter elements targeted by plastid sig-
nal transduction pathways evolved before LREs. Therefore, it is possible that
photoreceptor-mediated transcriptional regulation was produced during evo-
lution by targeting, either directly or through new regulators (i.e. via protein-
protein interactions), the same transcription factors and cis-regulatory elements
that mediated the influence of chloroplasts on PhANGs transcription. This pos-
sibility is attractive because it suggests a simple mechanism by which different
gene families whose expression is coordinate could simultaneously acquire a
new, coordinated pattern of regulation.
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CONCLUDING REMARKS
Much remains to be learned about the structure, mode of action, and evolu-
tion of LREs. It is clear that LREs are complex, composed of at least two
cis-acting elements, that can be targeted by different photoreceptor-activated
signal transduction pathways. The composite and variable structure of LREs
could explain the specific properties of individual light-responsive promoters.
Phylogenetic analysis of LREs clearly indicates that they have evolved from
ancient regulatory elements, whose original, primary function was probably
not light regulation. Transformation of mosses and other nonflowering plants
in which the expression of photosynthesis-associated genes is not regulated by
light could help in answering some questions concerning the evolution of LREs
and the different signal transduction pathways that activate them. It will be of
great interest to explore how a new mode of regulation, affecting many gene
families involved in photosynthesis, arose during evolution.
A
CKNOWLEDGMENTS
We are grateful to June Simpson for critical reading of this manuscript. This
work was supported by a grant from the HHMI to LH-E (75 197-526902).
Visit the Annual Reviews home page at
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