LIGHT CONTROL OF SEEDLING DEVELOPMENT 217 Possible Roles of Plant Hormones........... .......................................................................... 231 Repressors of Light-Mediated Development....................................................................... 232CONCLUSION.............................................. .......................................................................... 235INTRODUCTION1Seed germination and seedling development interpret the body plan with itspreformed embryonic organs, the cotyledons, the hypocotyl, and the root.Whereas embryo and seed development take place in the shelter of the paren-tal ovule, rather independently of the environmental conditions, seed germina-tion and seedling development are highly sensitive and dramatically respon-sive to environmental conditions. Higher plants have evolved a remarkableplasticity in their developmental pathways with respect to many environ-mental parameters. First, the embryonic axes of the root and the shoot orientthemselves in opposite directions in the field of gravity. Second, seedling de-velopment is highly responsive to light fluence rates over approximately sixorders of magnitude. The direction of incident light entices shoots and roots torespond phototropically. Light intensity and wavelength composition are im-portant factors in determining the speed of cell growth, of pigment accumula-tion, and of plastid differentiation. Angiosperms, in particular, choose between two distinct developmentalpathways, according to whether germination occurred in darkness or in light.The light developmental pathway, known as photomorphogenesis, leads to aseedling morphology that is optimally designed to carry out photosynthesis.The dark developmental pathway, known as etiolation, maximizes cell elon-gation in the shoot with little leaf or cotyledon development as the plant at-tempts to reach light conditions sufficient for photoautotrophic growth. Al-though the exact patterns of seedling morphogenesis vary widely among dif-ferent taxa, the light-regulated developmental decision between the etiolatedand the photomorphogenic pathway transcends phylogenetic classification.Arabidopsis thaliana, for example, is programmed to switch between the pho-tomorphogenic and the etiolation pathway in the hypocotyl and the cotyle-dons. In the legumes, such as Pisum sativum, which use the cotyledons asstorage organs, the corresponding developmental switch is programmed in theepicotyl and the primary leaves. Comparable phenomena of developmentalplasticity are observed in the mesocotyl, the coleoptile, and the first leaf ofmonocotyledonous seedlings such as oat and rice (50, 99, 136). It is reason-able to speculate that the fundamental mechanism is similar in different plant1 Abbreviations: UV-A, 320–400 nm light; UV-B, 280–320 nm light; HIR, high-irradiance re-sponse; LF, low fluence response; VLF, very low fluence response; Pr, phytochrome form withabsorbance maximum in the red; Pfr, phytochrome form with absorbance maximum in far-red.We follow the phytochrome nomenclature proposed in Reference 141.
218 VON ARNIM & DENGspecies, though defined light signals are frequently coupled to individual re-sponses in a species-dependent manner. The contrasting developmental patterns are thought to be mediated primar-ily by changes in the expression level of light-regulated genes (reviewed in 5,90, 168). The cellular events leading to the activation of these genes havebeen studied intensively, and extensive progress in elucidating some of thedownstream steps in phytochrome and blue light receptor signaling has beenreviewed during the past two years (15, 115, 138, 140, 152). Use of Arabidop-sis thaliana as a model organism has led to profound advances in understand-ing the light control of seedling development. We attempt to put these recentgenetic advances in perspective with traditional physiological data from otherspecies and focus on the overlap and the mutual fertilization between thesetwo lines of research. Many valuable perspectives on photomorphogenesis have been describedin a series of recent reviews on, for example, responses to blue light (75, 97),responses to UV light and high light stress (7, 40), ecological considerations(154, 155, 157), progress based on transgenic plants (188), phytochrome(138–140, 157, 176, 177), and mutational analysis (28, 45, 78, 86, 97, 134,143, 188).COMPLEXITY OF LIGHT RESPONSES ANDPHOTORECEPTORSIn a given species, the specific effects of light can differ drastically from oneorgan or cell type to the other and even between neighboring cells. In Arabi-dopsis, light treatment of a dark-grown seedling will reduce the cell elonga-tion rate in the hypocotyl while inducing cell expansion and cell division inthe cotyledon and the shoot apex. Meanwhile, stomata differentiation is pro-moted by light in both the growth-arrested hypocotyl and the expanding coty-ledon. In light-exposed shoots, plastids differentiate from proplastids or etio-plasts into chloroplasts, whereas in the adjacent cells of the root, plastids dif-ferentiate instead into amyloplasts under both light and dark conditions. Light responses are also known to exhibit fundamental changes in sensitiv-ity as development progresses, e.g. from responsiveness to red light to bluelight. This effect is conceptually most easily demonstrated at the level of geneexpression (18, 61, 64, 73). Finally, the kinetics of light-mediated effects allow for fast responses (inminutes), such as the inhibition of hypocotyl elongation (37, 162) or the in-duction of early light-inducible transcripts (114), but also accommodate slowresponses (from hours to days), e.g. the entrainment of circadian rhythms bylight (3a, 12, 103, 106, 121, 192).
LIGHT CONTROL OF SEEDLING DEVELOPMENT 219 Perhaps the most important component for encoding the complexity of re-sponses is the multiple families of photoreceptors. Seedling responses to lightare mediated by at least three classes of regulatory photoreceptors: (a) phyto-chromes, which respond mainly to red and far-red light but which also absorbblue and UV-light; (b) photoreceptors that are specific for blue and UV-Alight; and (c) UV-B photoreceptors. Photosynthetic pigments, for examplechlorophylls and carotenoids, have important roles as screening agents for theregulatory photoreceptors. Surprisingly little is known about their direct ef-fects on developmental responses (169). Molecular cloning of the Arabidopsis CRY1/HY4 gene (3, 91a, 91b, 103a)as well as characterization of photoreceptor mutants (80, 81, 83, 92) may helpto reveal the well-kept secrets of the blue light photoreceptors, which havelong been referred to as “cryptochromes.” The basis for the wide absorptionband of CRY1 in the blue and UV-A region of the spectrum has been resolvedby molecular analysis, which showed that CRY1 can bind two types of chro-mophores simultaneously, a flavin and a pterin (91b, 103a). It is conceivablethat both chromophore binding sites can be mutated independently, thus sepa-rating sensitivity to UV-A and blue light genetically, as has been demon-strated in Reference 191. In Arabidopsis (3, 87), and also in transgenic to-bacco (103a), CRY1 is responsible for sensitivity of hypocotyl elongation togreen light, in addition to blue and UV-A. A possible explanation is providedby the tendency of CRY1 to stabilize a reduced, green-light absorbing form ofthe flavin chromophore (91b). The phytochromes (phys), a family of dimeric, approximately 240-kDachromoproteins, are by far the best studied of all photoreceptors (62, 138–141,176, 177). In all known phytochromes, absorption of light leads to a confor-mational shift (photoconversion) of a red light absorbing form (Pr, absorptionmaximum around 660 nm) into a form with increased sensitivity to far-redlight (Pfr, 730 nm). Absorption of far-red light converts the molecule back tothe Pr form. Overlap in the absorption spectra of Pr and Pfr ensures that nolight condition can convert all phytochrome into exclusively one form. Onlyphytochrome that is newly synthesized in complete darkness is present exclu-sively as Pr. It is generally approximated that the concentration of Pfr, ratherthan Pr, is responsible for all of the photomorphogenic effects of phyto-chrome, although this view has recently been challenged (95, 142, 151, 154). Phytochrome responses allow an operational distinction among differentlevels of sensitivity: Low fluence (LF) responses are saturated by pulses witha red fluence component of 1 to 1000 µmol photons/m2. They are at least par-tially reversible by a subsequent far-red light pulse. The effectiveness of thefar-red pulse is a function of the intervening period of darkness. This functionis known as the escape kinetic, a powerful tool to probe the chain of down-stream signaling events. Very low fluence (VLF) responses (<1 µmol/m2 red)
220 VON ARNIM & DENGare inducible by pulses of far-red light alone. High-irradiance responses (HIR)(typically >1 µmol/m2/s) require continuous irradiation, which precludesanalysis of far-red reversibility. Phytochrome apoproteins are encoded by a small gene family with fivemembers in Arabidopsis (PHYA, PHYB, PHYC, PHYD, and PHYE) (34, 139).Typically, phytochrome A (phyA) holoprotein is abundant in etiolated tissueand is greatly reduced in green tissue because it is degraded with a half life ofapproximately 1 h when in the Pfr form (177). Expression of the PHYA genein Arabidopsis and some other species is downregulated by light (38, 66, 149,159). PHYB, C, D, and E are moderately expressed in both etiolated and greentissues (34, 141, 158). Mutational analysis has revealed that phyA and phyBhave distinct, partially complementary and partially overlapping functions inArabidopsis (31, 71, 140, 142, 154, 155, 188). The absorption spectra of atleast phyA and phyB appear to be almost identical and can therefore not be re-sponsible for the different physiological functions (179, 180). In addition, thephytochromes that have been examined at the seedling stage seem to be ex-pressed ubiquitously, albeit at different levels, and may contribute only quan-titatively to the tissue specificity of many light responses (1, 34, 158). Functionally distinct phytochromes have been similarly observed in manyother species (139, 188). Apart from Arabidopsis (Table 1) (86, 87), mutantsdeficient in specific phytochromes have been described in cucumber (lh) (2,102), Brassica (ein) (49), pea (lv) (186), tomato (85) (tri) (172, 173), and sor-ghum (27).RESPONSESSeed GerminationSeminal experiments on the light control of seed germination and its actionspectrum revealed the photoreversibility of the phytochrome photoreceptor(13, 153). The recent availability of mutants affecting specific phytochromesin Arabidopsis has allowed a critical evaluation of the roles of individual phy-tochromes on seed germination (35, 142, 151). Rapid germination of Ara bi-dopsis seeds imbibed in darkness is controlled primarily by phyB, stored inthe Pfr form (PfrB) in the seed, whereas phyA contributes little to the decisionto germinate in darkness. The seed germination rate in darkness is particularlyhigh in seeds overexpressing phyB (108). Moreover, short pulses of red lightincrease the germination efficiency of the wild type further, which suggeststhat a significant level of phyB is also present in the Pr form in at least a frac-tion of seeds (151). A prominent role for a light-stable phytochrome such asphyB is consistent with the slow escape of the red response from reversibilityby a pulse of far-red light (14).
LIGHT CONTROL OF SEEDLING DEVELOPMENT 221Table 1 Arabidopsis mutants defective in aspects of photomorphogenesisaName Other names Gene Phenotype References clonedMutants in photoreceptor apoprotein genesphyA hy8, fre1 Yes long hy in FR 41, 120, 133, 142, 189phyB hy3 Yes long hy in R and W 87, 118, 142, 160cry1 hy4 Yes long hy in B and W 3, 87, 91a,b, 98, 103aMutants in genes for pleiotropic regulators Negative regulators cop1 to fus 12 in D:cop1 fusl, embl68 Yes –short hy 46–48, 112, 116cop8 fus8, embl34 No –open cotyledons 116, 185cop9 fus7, embl43 Yes –green root 116, 183, 184cop10 fus9, embl44 No –thylakoid membranes 116, 185cop11 fus6, emb78 Yes –cell differentiation 24, 116, 185detl fus2 Yes –derepression of light- 30, 32, 33, 116, 135 inducible genesfus4, -5, No 88a, 116-11, -12 Positive regulatorsfhy1, fhy3 No long hy in FR 189hy5 No long hy under R and B 87Mutants in genes regulating specific responses Negative regulatorsamp1 No hook open, derepressed gene 25 expression in Dcop2 No hook open 68cop3 hls1 No hook open 51, 68cop4 No de-etiolated, nuclear gene 68 expression agravitropicdet2 No de-etiolated, nuclear gene 29 expressiondet3 No short hy, open cotyledons 19adoc1–doc3 No elevated CAB 89 expression in Dgun1–gun No nuclear gene expression 1653 uncoupled from plastidicx1 No CHS expression sensitized to 68a light Positive regulatorscue1 No low CAB expression 89a
222 VON ARNIM & DENGTable 1 (continued)Name Other names Gene Phenotype References clonedPhototropism mutantsnph1 JK224 No nonphototropic 80, 81, 83, 92nph2, nph4 No “-” 92nph3 JK218 No “-” 80, 81, 92rpt1–rpt3 No nonphototropic 129–131 root Abbreviations: hy, hypocotyl; FR, far-red light; R, red light; B, blue light; W, white light; D, dark-ness; CAB, chlorophyll a/b–binding protein gene; CHS, chalcone synthase gene. Other phytochromes, such as phyA, gradually accumulate in the imbibedseed, promoting germination particularly under continuous far-red light. Un-der far-red light, phyB mutant seeds germinate more efficiently than wildtype. Thus, the wild-type PHYB allele appears to negate the action of phyA,which provides an example for antagonistic control of the same response bythe two types of phytochrome (142, 151). Because the inhibitory effect ofPHYB is clearly retained in the phyA mutant (142), phyB probably does notact directly on phyA but rather on a downstream effector of phyA. The levelof PfrB is extremely low in far-red light and suggests that the negative effectof phyB on phyA-mediated seed germination may be conferred by its Pr form(142, 151).Sketch of Seedling PhotomorphogenesisSeedling development in complete darkness differs markedly from that incontinuous white light or under a light-dark cycle. Under light conditions, theArabidopsis seedling emerges from the seed coat, consisting of a hypocotylwith an apical hook, two small folded cotyledons, and a short main root. Afteran initial increase in volume, which is attributable primarily to hydration, theapical hook starts to straighten, and, at the same time, the cotyledons open andexpand by cell division and cell expansion, accompanied by chlorophyll accu-mulation and greening. Meanwhile, the apical meristem gives rise to the firstpair of true leaves, which carry trichomes. The hypocotyl translates positivephototropic and negative gravitropic cues into growth by differential cellelongation, in order to position the cotyledons for optimal exposure to thelight source. In contrast, the root interprets the same signals in exactly the op-posite manner, showing positive gravitropism and negative phototropism. In darkness, the embryonic organs develop according to a completely dif-ferent program. After an initial phase of moderate cell expansion due to hy-dration, the hypocotyl cells elongate rapidly while the apical hook persists for
LIGHT CONTROL OF SEEDLING DEVELOPMENT 223over a week and the cotyledons remain folded. The apical meristem remainsarrested in the dark. Only gravitropic cues position the hypocotyl upright inanticipation of a light source. At the subcellular level, plastids undergo drastic changes in morphologyand protein composition in both darkness and light. In darkness, proplastids inthe cotyledons develop into etioplasts, characterized by a paracrystalline pro-lamellar body and a poorly developed endomembrane system. Upon exposureto light the prolamellar body quickly disappears and is replaced by an exten-sive network of unstacked and grana-stacked thylakoid membranes, similar tothose of the light-grown seedlings. In contrast with the aerial portion of the seedling, roots develop in a similarpattern in both light and darkness. During the first week of seedling develop-ment, chloroplast development remains repressed under both light and darkconditions. However, if plants continue to expose their roots to light beyondthe seedling stage and into adulthood, chloroplast development can be ob-served in the older part of the root system.Formation of New Cell TypesUnder laboratory conditions, light-dependent decisions that affect cell shapeand differentiation during Arabidopsis seedling development only become ap-parent two days after germination and then lead quickly into diverging path-ways (185). The first two days in light or darkness are accompanied by overallcell enlargement in hypocotyl, root, and cotyledon, and root hairs develop.During the following day in darkness, hypocotyl cells elongate enormously,and the hypocotyl epidermis forms a smooth surface. In the light-grown sib-ling hypocotyl, cell enlongation is inhibited and cell-type differentiation pro-ceeds. The most obvious examples are the initiation and maturation of stomatain the epidermal layer of the hypocotyl, which are absent from the hypocotylin the dark (185). In Arabidopsis, epidermal hairs are confined to true leaves,which are themselves dependent on light. The related crucifer Sinapis alba(white mustard), however, shows that differentiation of epidermal hairs on thehypocotyl can be under direct light control (181). The cotyledon development in darkness is essentially arrested after twodays, whereas in the light, cotyledon cells differentiate into distinct cell types,such as vascular, mesophyll, and epidermal cells. The most conspicuouschange in the expanding mesophyll cells is the differentiation of numerousproplastids into green chloroplasts, although little differentiation betweenpalisade and spongy mesophyll cells occurs (32, 46). Meanwhile, the epider-mal pavement cells expand into their characteristic lobed, jigsaw puzzleshape. A set of guard-cell initials is present in the embryonic cotyledons andwill differentiate into guard-cell precursors regardless of light conditions dur-ing the first two days (185). While development of guard-cell precursors then
224 VON ARNIM & DENGarrests in darkness, it continues to completion under light conditions. In addi-tion, only in the light-grown cotyledons do new guard-cell initials form, fol-lowing polarized cell divisions of epidermal cells (185). Finally, the vascula-ture in dark-grown seedlings is rather undeveloped but is quite extensive inlight-grown seedlings. This has been clearly documented in Zinnia seedlingsby using three early markers for developing xylem and phloem cells (44).Cell Autonomy and Cell-Cell InteractionsWhat is the role of cell-cell communication and the extent of cell autonomyduring the light control of seedling development? After microinjection of phy-tochrome into tomato hypocotyl cells, it was shown that the anthocyanin accu-mulation and the phytochrome-mediated gene expression pathways are cellautonomous (123). Similar conclusions were reached for the anthocyanin ac-cumulation pathway by irradiating mustard cotyledons with a microbeam ofred or far-red light (124). Microirradiation at one site, specifically on a vascu-lar bundle or on a site in the lamina, could suppress anthocyanin accumulationat a site distant from the irradiated site, such as the leaf margin. This demon-strates that long-range inhibitory signals are transmitted through the leaf uponirradiation (124). Even under uniform irradiation, individual cells in the mus-tard cotyledons responded in an all-or-none fashion, which resulted in patchypatterns for both anthocyanin synthesis and for the mRNA of the key enzymechalcone synthase (CHS). However, only a subset of those cells that accumu-lated CHS mRNA accumulated a significant level of anthocyanin. This indi-cates that, in addition to CHS mRNA, additional rate-limiting factors must bedistributed unevenly over the leaf as well. If those factors are themselveslight-dependent, then the mustard seedling’s competence for the stochasticpatterning may be interpreted as a means to preserve responsiveness over awide range of fluence rates, which is typical for light responses in plants(124).Unhooking and Separation of the CotyledonsThe separation of the cotyledons and the opening of the apical hook are stimu-lated by red light (23, 94); in some species, such as Arabidopsis, hook openingis also promoted by far-red or blue light, which indicates that multiple photo-receptors mediate this response (94, 96). Cotyledons that are folded back onthe hypocotyl are formed initially during the late stage of embryogenesis, andthe apical hook is maintained at the top of the hypocotyl during etiolation. Adevelopmental problem is that the hypocotyl, but not the hook, responds to di-rectional light with differential cell elongation and phototropic curvature,while the hook manages to perform differential cell elongation in the com-plete absence of any directional light signal. Mutations in a number of Arabi-dopsis loci, such as hookless1 (hls1)/constitutively photomorphogenic 3
LIGHT CONTROL OF SEEDLING DEVELOPMENT 225(cop3), amp1, and cop2 (25, 51, 68), result in a loss of the apical hook in dark-ness. On the other hand, mutation to ethylene overproduction (eto) or to a con-stitutive ethylene response (ctr1), or external application of ethylene, all resultin an exaggerated hook. Therefore it is likely that ethylene, perhaps in con-junction with auxins, is required to maintain the apical hook (51). The effectof ethylene on hook formation may well be counterbalanced by cytokinins, assuggested by the hookless phenotype of the cytokinin overproducing mutantamp1 (25), although external application of cytokinins can also facilitate hookformation via ethylene (21). Light, however, overrides the effect of the ethyl-ene signal (82). In Arabidopsis, the response of the hook to both low fluence red and bluelight is phytochrome mediated and far-red reversible, whereas intense far-redand blue light act through high-irradiance responses, which lack fluence reci-procity and far-red reversibility (94, 96). The latter involve phyA and a bluelight–specific pathway that is also involved in hypocotyl elongation (97). Dur-ing the transition of dark-grown seedlings to light, unhooking and arrest of hy-pocotyl elongation follow similar fluence rate-response curves in Arabidopsis(94). Both also require a functional HY5 gene (96) and may therefore dependon similar signal transduction pathways, but in other species the two processesare more easily separated (94).Cotyledon Development and ExpansionThe same light signals that inhibit cell elongation in the hypocotyl also pro-mote cell expansion in the cotyledons and the leaf. How these differential re-sponses to the same light environment are regulated remains poorly under-stood (39, 50, 174, 175). Blue and red light–mediated leaf expansion beginsafter distinct short and long lag times, respectively, in leaves of Phaseolus,which is reminiscent of the short and long lag times that pass between blueand red irradiation, respectively, and the inhibition of hypocotyl cell elonga-tion in cucumber (10, 37). Perhaps promotion and inhibition of cell expansionare induced by similar pathways in the two organs. Under white light, phyto-chromes A and B appear almost dispensable individually for cotyledon expan-sion in Arabidopsis (142). Full cotyledon expansion in bright red and bluelight, however, depends on signals perceived by phytochrome B, as indicatedby reduced cotyledon expansion in the phyB mutant (142). This phytochrome-B-mediated cotyledon expansion is organ autonomous (122). The cry1/hy4mutants show a decrease in cotyledon expansion, which confirms the involve-ment of a blue light receptor (11, 87, 93). Detaching the cotyledons from thehypocotyl rescues the cotyledon defect of cry1/hy4 in blue light, suggestingthat the cry1/hy4 mutant hypocotyl may exert an inhibitory effect on cotyle-don expansion (11). The importance of light perception in the hypocotyl or thehook for events in the cotyledons (126), and vice versa (9), has long been
226 VON ARNIM & DENGknown. Overexpression of the photomorphogenic repressor COP1 leads to aninhibition of cotyledon cell expansion under blue light only, similar to the ef-fect in cry1/hy4 (113). This result indicates that COP1 contributes to the inhi-bition of cotyledon cell expansion that is alleviated by CRY1/HY4 activity.Inhibition of Hypocotyl ElongationThe inhibition of hypocotyl elongation in response to illumination is one ofthe most easily quantifiable developmental processes and has greatly facili-tated our understanding of the roles of regulatory components (16, 65, 85, 87,93, 113, 182). Inhibition of hypocotyl elongation shows a complex fluence de-pendence that combines inductive, i.e. phytochrome-photoreversible (50,127), and high-irradiance responses (HIR) (6, 89, 191). The considerablequantitative variation in the spectral sensitivity among different species is noteasily explained (104). Multiple photoreceptors can control hypocotyl elongation, although withdistinct kinetics. In cucumber hypocotyls, for instance, cell wall extensibilityand subsequent cell elongation are inhibited extremely rapidly in response toblue light, starting after a lag of less than 30 s (37, 161, 162). Such a fast re-sponse is unlikely to require gene expression. Following a lag of over 10 min,the phytochrome-mediated response is considerably delayed (157). In Arabidopsis, phytochromes A and B, the blue light receptor CRY1/HY4and a genetically separable UV-A receptor have been shown to contribute tothe inhibition of hypocotyl cell elongation (65, 87, 188, 191). Different from,for example, Sinapis alba, which is most sensitive to red and far-red light (6,67), Arabidopsis hypocotyl elongation is most easily inhibited under bluelight, where phytochromes and blue light receptors appear to act additively,specializing in low and high fluence responses, respectively (97, 91a).Whether the species-specific differences in sensitivity reflect subtle differ-ences in the spectral properties or concentrations of the photoreceptors, thelight environment inside the plant tissue, the mutual coupling of different pho-totransduction chains, or merely differences in the experimental protocol re-mains to be addressed. Arabidopsis phyB mutants show a moderately elongated hypocotyl underwhite light (87, 118, 144, 160), where phyA mutants exhibit no such defect(41, 120, 133, 189). A drastic exaggeration of the long hypocotyl phenotype isseen in phyA/phyB double mutants (142). Therefore, under white light, inhibi-tion of hypocotyl elongation can be mediated not only by blue and UV-A lightbut also by both phyA and phyB in an arrangement suggesting multiple, butonly partially redundant, control (22, 140, 142). Under continuous red light, phyB is the active phytochrome species inhib-iting hypocotyl elongation, whereas under continuous far-red light, phyA isprimarily responsible. However, supplementing a seedling growing in con-
LIGHT CONTROL OF SEEDLING DEVELOPMENT 227stant red or white light with far-red light causes the hypocotyl to elongatemore rapidly than in constant red or white or in far-red light alone (110, 190).This effect is apparent in many species and is part of the “shade avoidance”response in adult plants, because a high ratio of far-red to red light is typicalfor the light environment under a plant canopy (154, 155). One simple model attempts to explain the rate of hypocotyl elongationsolely on the basis of the distinct steady-state levels of PfrB and PfrA, as esti-mated from their differential stability and expression levels: As discussed inthe section on Complexity of Light Responses and Photoreceptors, phyB isrelatively stable as Pfr and is expressed continuously at a moderate level,fairly independent of light. In contrast, phyA expression is high in darknessand low in the light, and PfrA is rapidly degraded (160, 177). Continuous red-light irradiation will therefore rapidly deplete the plant of phyA but not ofphyB. Little phyA-mediated signaling is expected under these conditions, andcontinuous red light effects are attributed mainly to phyB. Continuous far-redlight, however, can lead to a relatively high steady-state level of PfrA andhence can cause a pronounced developmental effect, because the low ratio ofactive Pfr to inactive Pr may be compensated for by the high overall phyAlevel. The low level of phyB in combination with the low Pfr-to-Pr ratiomakes signaling through phyB negligible under the continuous far-red light.This model approximates the different roles of phyA and phyB on the basis oftheir expression levels and degradation rates alone and does not take into ac-count some possible differences in the coupling of phyA and phyB to regula-tors or downstream effectors. Consistent with the overlapping roles of phyA and phyB as inferred frommutant analysis, overexpression of cereal phyA in tobacco (26, 72, 76, 77,107, 110, 111, 119), tomato (16), and Arabidopsis (17) or of phyB in Arabi-dopsis (108, 180) increases the seedlings’ sensitivity to light, as judged by anextremely short hypocotyl under white light. Overexpression of heterologousphyA increases the sensitivity to far-red, white, and red light, which suggeststhat the elevated level of phyA persists even under prolonged irradiation withred light, a condition that leads to rapid degradation of the endogenous phyA(16, 25, 110, 111, 119). On the other hand, is sensitivity to far-red light alsoincreased in seedlings overexpressing the photostable phyB? Such an increasewould be expected according to the model put forward, on the basis of the es-sentially identical absorption spectra of phyA and phyB. However, this doesnot seem to be the case. Overexpression of phyB does not sensitize hypocotylinhibition to far-red light (108, 109, 187). Therefore, phyA and phyB may in-teract with distinct sets of regulator or effector molecules. Similarly, phyBoverexpression does not disable the shade avoidance response in adult plants,in contrast with the effect of phyA (110).
228 VON ARNIM & DENGPhototropismSeedlings of higher plants orient their growth with regard to the direction oflight in an attempt to optimize exposure of the photosynthetic organs to light(55). The phototropic curvature of the shoot is achieved by differentialgrowth, with cells on the shaded side elongating more strongly than cells onthe surface exposed to light. Phototropism in Arabidopsis is superimposedover the light inhibition of hypocotyl elongation and over the negative gravi-tropic regulation of cell elongation in the hypocotyl (19). Therefore, a singlecell elongation event may integrate signals from three different transductionchains simultaneously. The role of light on tropic responses is complicatedfurther by the interaction of a phytochrome-mediated pathway with the gravi-tropic pathway in both the hypocotyl (63) and the root (54, 95). Typically, phototropism is mediated by blue and UV-A light, but greenlight is effective in Arabidopsis as well (163). Red light absorbed by phyto-chrome stimulates phototropism directly in pea (132) and modulates the pho-totropic response to blue light in Arabidopsis (69, 70). Transduction of photo-tropic stimuli involves an early phosphorylation of a 120-kDa membrane-associated protein (152). Mutational analysis has identified four complemen-tation groups of nonphototropic hypocotyl (nph) mutants (80, 92) and threecomplementation groups for root phototropism (rpt) mutants (129–131). Mutants defective in blue light–mediated hypocotyl cell elongation (cry1/hy4) retain normal phototropic responses, and phototropic mutants (JK218/nph3 and nph1-1) respond normally to light by inhibition of hypocotyl cellelongation. Those results not only confirm that the two processes are geneti-cally separable but also suggest that they are almost certainly mediated by dis-tinct photoreceptors (92, 98), because CRY1/HY4 encodes a blue light recep-tor (3) and nph1 mutants are defective in an early signaling step of blue andgreen light–mediated phototropism, most likely light perception (92). A con-ceptual similarity among the distinct roles of individual phytochrome familymembers and the members of the family of blue light receptors becomes ap-parent. Although nph1 mutants are defective in both shoot and root phototropism,other phototropism mutants, such as rpt1 and rpt2, are specifically defectivein root—but not shoot—phototropism only (129, 130). This suggests thatnph1-mediated signals can be fed into at least two different pathways, depend-ing on cell type, and that the signaling mechanisms in shoot and root are dis-tinct. In support of this interpretation, shoot but not root phototropism is re-sponsive to green light in Arabidopsis (131). Plant hormones, especially auxins, have been implicated in differential cellelongation processes, such as during phototropism and gravitropism in hypo-cotyls, coleoptiles, and roots. Whether phototropism requires redistribution ofauxins or modulation of auxin sensitivity is not well established (55, 125,
LIGHT CONTROL OF SEEDLING DEVELOPMENT 229130), but investigation of phototropism in auxin-deficient, resistant, or over-producing strains could differentiate between different models. In fact, be-cause the phototropic response is unaffected by the auxin resistance mutationaux1 (130), root phototropism may not necessarily be compromised by de-fects in auxin signaling. Roots and hypocotyls of Arabidopsis also exhibit differential cell elonga-tion responses after gravitropic stimulation (129). Phototropism mutants nowenable us to dissect the relationship between phototropism and gravitropismin Arabidopsis roots. Roots exhibit positive gravitropism and negative photot-ropism, and both responses rely on differential cell elongation. Three mutantshave been described that affect both photo- and gravitropism (80, 81), butmany mutations that affect one of the responses specifically are available.Both rpt1 and rpt2 have apparently normal shoot gravitropism, which alsosuggests that a specific signaling pathway for light exists in the root. How-ever, the agravitropic mutants aux1 and agr1 show normal root phototropism(130). In the shoot, photo- and gravitropism are clearly separable genetically,because four different nph mutants, including nph1, are gravitropically nor-mal (92). Previous photophysiological analysis demonstrated separate photoreceptorsystems for blue/UV-A light (PI) and green light (PII) (75, 83, 84), but an alle-lic series of nph1 mutants suggests a new interpretation. The weak allelenph1-2 (JK224) is merely defective in first (low light) positive phototropismin blue light but is wild-type-like in green light, whereas more severe alleles,for example nph1-1, are additionally defective in second positive curvature inboth blue light and green light. The allelic series of NPH1 indicates that bothtypes of signals are processed by a single gene product for a photoreceptorapoprotein, possibly carrying two independently disruptable chromophores orone chromophore in alternative chemical states (92). In this respect it is inter-esting to note that the CRY1/HY4 gene product may also bind two distinctchromophores, namely a pterin and a flavin (3, 91b, 103a). A detailed com-parison of the relationship between the two photoreceptor systems awaits mo-lecular analysis of the NPH1 gene.Plastid DevelopmentChlorophyll accumulation and the concomitant transition of the proplastid oretioplast to the chloroplast are arguably the most striking responses to lightand certainly require the intricate cooperation between multiple biochemicalassembly and disassembly processes. In several species, pretreatment with redlight, perceived at least partially by phyA and phyB, potentiates the accumula-tion of chlorophyll (74, 91). A feedback mechanism that conditions nucleargene expression for a subset of plastid proteins operates via a biochemicallyundefined plastid signal, which is depleted by photooxidative damage to the
230 VON ARNIM & DENGplastid (36, 166, 167). At least part of this regulatory circuit involves an in-hibitory element, because nuclear gene expression has escaped from the con-trol by the plastid in recessive mutant alleles of at least three Arabidopsiscomplementation groups (GUN1–GUN3) (165). These mutants have few mor-phological defects, but have the tendency to green inefficiently when they aretransferred from darkness to light in the etiolated state (165). Mutant analysis has further demonstrated a panel of negative regulators,which keep chloroplast development suppressed in the cotyledons of dark-grown seedlings. Mutations at each of 10 loci known as Constitutively Photo-morphogenic (COP1, COP8–COP11), De-etiolated (DET1), and Fusca(FUS4, 5, 11, and 12) result in the absence of etioplasts and in partial chloro-plast development in complete darkness, accompanied by cotyledon expan-sion, arrest of hypocotyl elongation, and light-specific cell type differentiation(24, 30, 32, 46, 48, 88a, 112, 116, 184, 185). The same loci also suppresschloroplast development in the roots of light-grown seedlings, because themutants’ roots develop chloroplasts and turn green. Mutations at several other loci affect overall organ development and ex-pression of light-inducible genes during seedling morphogenesis without re-sulting in plastid differentiation. For examples, cop4 and det2, both of whichdisplay significant derepression of light-inducible genes in darkness, have noimpact on chloroplast development (29, 68). A group of mutants at three loci,known as DOC1, DOC2, and DOC3 (dark overexpressors of CAB) accumu-late mRNA from the chlorophyll a/b binding protein gene (CAB) promoter indarkness, without a conspicuous morphological phenotype (89). The comple-mentary mutant phenotype, namely opening of the cotyledons on a short hy-pocotyl accompanied by continued repression of light-inducible genes indarkness, has been described for the det3 mutant (19a). In this mutant chlor-plast, development remains tightly controlled by light. The particular combinations of phenotypic defects in the various mutantsdescribed to date present a dilemma for the geneticist, because no simple lin-ear sequence of gene action is consistent with all the data. While it is temptingand straightforward to invoke feedback circuits in order to solve the problem,detailed evidence for them is scarce. Elucidating the logic of the light signaltransduction events may therefore require the mechanistic dissection of thefunction of the various gene products.REGULATORS OF LIGHT RESPONSES IN SEEDLINGSPositive RegulatorsIt is a recurring theme that predominantly negative regulators of photomor-phogenic seedling development are uncovered in various genetic screens,
LIGHT CONTROL OF SEEDLING DEVELOPMENT 231whereas genetic identification of the positive regulators is sparse (see Figure1) (28, 45). The prevalent coaction between pigment systems (52, 70, 117, 128, 171)and, in particular, the partial redundancy inherent in multiple photoreceptorsystems may be two reasons for the difficulty of establishing mutants in posi-tive regulators. Remarkable exceptions are the genes FHY1 and FHY3, whichresult in phenotypes similar to phyA mutants. These gene products may actdownstream of PHYA in transmitting a signal specific for phytochrome A (71,189). A fruitful approach to identifying specific regulators genetically may in-clude screening for modifiers, suppressors or enhancers, of established photo-morphogenic mutations. As an example, a suppressor of the Arabidopsisphytochrome-deficient hy2 mutation (shy1) with some specificity for sup-pressing the phenotype under red rather than far-red light has been uncovered(BC Kim, MS Soh, BJ Kang, M Furuya & HG Nam, personal communica-tion). A second promising line of research is to screen for mutants defective inthe light-dependent expression of specific genes. Following this rationale,the CUE1 gene has been identified as a positive regulator of light-dependentnuclear and plastid gene expression (89a). Similarly, expression of the genefor chalcone synthase (CHS) and genes for related enzymes in the antho-cyanin synthesis pathway is sensitized to light in the Arabidopsis mutant icx1(68a). The HY5 gene product integrates signals from multiple photoreceptors tomediate inhibition of hypocotyl cell elongation in response to blue, red, andfar-red light, but not UV-B light (4, 28, 87). These light conditions have alsobeen shown to cooperate in abolishing the activity of COP1, a negative regu-lator of light responses (113). Mutations of COP1 and the positive light regu-latory component HY5 exhibit an allele-specific interaction. Although a strongallele of cop1 is epistatic over a mutant hy5 allele, hy5 can suppress the phe-notype of the weak allele cop1-6. The suppression of the cop1-6 phenotype byhy5 could be attributed to compensating alterations in the surfaces of two in-Figure 1 Scheme change of the sequence of events leading from light perception to developmentalresponse. Examples for relevant gene products that have been identified by mutation are indicated.Please note that developmental and hormonal signals can modulate the light response by affectingany step of the sequence.
232 VON ARNIM & DENGteracting proteins (4). Molecular cloning of the HY5 gene should allow a di-rect test of this hypothesis.Possible Roles of Plant HormonesMany of the light-regulated seedling developmental responses, such as the in-hibition of hypocotyl cell elongation (21, 101, 150), stem elongation (8), thecell division in the shoot apex (33), opening of the apical hook (51), and theinduction or repression of nuclear gene expression, also respond to treatmentwith one or more of a variety of plant hormones (38, 42, 56). We have brieflyalluded to possible contributions of ethylene and auxins to the control oftropic responses (51, 55, 125, 130). The question arises how hormonal andlight effects are integrated with each other: Are hormones second messengersin light responses? Or do they transmit another signal that shares a commontarget with light? Or do they serve as integrators of distinct signaling path-ways by “cross talk?”CYTOKININS The relationship between light on the one hand and cytokininsand giberellins on the other has received the most thorough attention. For exam-ple, control of a wheat kinase gene homolog (WPK4) by light may require thepresence of cytokinin, because a putative cytokinin antagonist (2-chloro-4-cyclobutylamino-6-ethylamino-s-triazine) specifically prevented the inductionof WPK4 mRNA (148). Even more intriguing is that de-etiolation of dark-grownArabidopsis seedlings can be mimicked partially by supplementing seedlingswith cytokinins under defined laboratory conditions (33). Moreover, the typi-cally light-inducible genes for a chlorophyll a/b binding protein (CAB) (64, 73)and for chalcone synthase (CHS) (53, 88) were moderately activated by cytoki-nin treatment, although the effective levels of applied cytokinins were about ten-fold higher than the endogenous level in these experiments. Tentative linksbetween a high cytokinin level and a suppressed etiolation response are sug-gested because of the correlation of a hook opening phenotype with a signifi-cantly elevated cytokinin level in the amp1 mutant, epistasis of amp1 over hy2(25), and the aberrant response of det1 and det2 to cytokinin (33). However, en-dogenous cytokinin levels in dark- and light-grown seedlings and in det1 anddet2 mutants were not consistent with the notion that light signals are transmit-ted simply by a change in cytokinin concentration (33). Furthermore, an addi-tive and probably independent co-action of cytokinin and light has beendemonstrated for the control of hypocotyl elongation (163a). Cytokinin may act posttranscriptionally on CAB mRNA levels in Lemnagibba, while light clearly has a transcriptional component, indicating inde-pendent and probably additive action of cytokinin and light (56, 57). Stimula-tory effects by moderate concentrations of applied cytokinins on the expres-
LIGHT CONTROL OF SEEDLING DEVELOPMENT 233sion of light-inducible, circadian clock–regulated genes have also been ob-served under light conditions, which again suggests additive effects (42, 43). In conclusion, although light effects may not be mediated primarily by cy-tokinin levels, any drastic alteration of the cellular cytokinin level by anystimulus other than light would be expected to modulate the seedling’s re-sponsiveness to light.GIBERELLINS Although both light and giberellins control hypocotyl elonga-tion, e.g. in cucumber (101), and mesocotyl elongation, for example, in rice(170), few genetic studies support the simple hypothesis that light acts throughaltering the levels of active giberellins (145–147). However, alterations in phy-tochrome levels have been shown to affect giberellin levels in tobacco (72), Sor-ghum (58, 59), and Brassica (49). One phenotype of the long hypocotyl mutantlh of cucumber, which has a deficiency in a B-type phytochrome and a constitu-tive shade avoidance response (100–102, 156), is an increase in the responsive-ness to giberellin. Conversely, in the wild type, depletion of Pfr increases theresponsiveness to giberellin (101). Phytochrome may similarly inhibit the sensi-tivity of the rice mesocotyl to giberellin (170). The careful dissection of the signaling chains for light on the one hand andhormones on the other by use of defined mutations and by molecular andphysiological analysis will allow researchers to pry apart the intertwined path-ways and will finally reveal the role of cytokinin, giberellins, and other hor-mones in the light control of seedling development.Repressors of Light-Mediated DevelopmentPLEIOTROPIC COP, DET, AND FUS GENES Combined efforts in photomorpho-genic mutant screens (cop or det mutants) and purple seed color screens (fuscamutants) have yielded a set of at least ten loci that are required for the full estab-lishment of the dark developmental pathway and suppression of photomorpho-genic development in darkness. The ten loci have been designated asCOP1/FUS1, DET1/FUS2, COP8/FUS8, COP9/FUS7, COP10/FUS9,COP11/FUS6, FUS4, FUS5, FUS11, and FUS12, and mutations in each resultin dark-grown seedlings with a pleiotropic de-etiolated or constitutively photo-morphogenic phenotype (24, 32, 46, 88a, 116, 184, 185). The mutants displaychloroplast-like plastids containing thylakoid membrane systems and lacking aprolamellar body in the dark-grown cotyledons and show a pattern of light-regulated gene expression in the dark resembling their light-grown siblings. Thewild-type COP/DET/FUS genes also contribute to the repression of photomor-phogenic responses in seedling roots under light conditions, because greeningand chloroplast development have been consistently observed in the light-grown mutants. The elevated expression of nuclear- and plastid-encoded light-inducible genes in the dark-grown mutants is a direct or indirect loss in the abil-
234 VON ARNIM & DENGity to repress nuclear gene promoter activity as indicated by analysis of trans-genic promoter-reporter gene fusions in the mutant backgrounds (29, 46, 184,185). Consistent with a widespread evolution of COP/DET/FUS-like functions,a pea mutant with light-independent photomorphogenesis (lip) has been de-scribed (60). On the basis of the recessive nature of those mutations and theirpleiotropic phenotype, it has been proposed that the photomorphogenic path-way constitutes the default route of development, whereas the etiolation path-way is an evolutionarily recent adaptation pioneered by the angiosperms (185). It is important to point out that for certain light-regulated processes, thepleiotropic COP/DET/FUS loci are clearly not required. For instance, severeloss-of-function alleles of all ten loci seem to retain normal phytochrome con-trol of seed germination (46, 88a, 185). The immediate downstream target of any of the COP, DET, and FUS re-pressor molecules remains unknown. It is possible that they directly inhibitthe transcription of photosynthetic genes or that they modulate expression ofan intermediate set of regulatory genes, which in turn regulate the final targetgenes. Some indirect evidence is consistent with the latter possibility. For ex-ample, COP1 is a regulator of the PHYA gene itself (46). Further, it was re-cently reported that the normally light-inducible homeobox gene ATH1 wasderepressed in dark-grown cop1 and det1 mutants (137). Together, ATH1 andtwo other homeobox genes, ATHB-2 and -4, exhibit light-regulated expressionpatterns (20, 137) and may act as downstream effectors of the COP/DET/FUSproteins. In addition, the DNA binding factor CA-1, which binds to a regionof the CAB promoter important for light regulation, was absent in the det1-1mutant allele, consistent with its function as a downstream target of inactiva-tion by DET1 (79, 164).OVEREXPRESSION STUDIES The molecular cloning of four pleiotropicCOP/DET/FUS loci (24, 47, 135, 183) permitted a direct test using overexpres-sion studies of the genetic model that their gene products act as repressors of thephotomorphogenic pathway. To date, overexpression of COP1 has producedthe clearest evidence for a photomorphogenic suppressor (113). Moderate two-to fourfold overexpression resulted in two responses typical for the etiolationpathway, namely, an elongation of the hypocotyl under blue and far-red lightand under a dark/light cycle and a reduction in cotyledon expansion under bluelight. These effects of COP1 overexpression under far-red or blue light resemblethose of the phyA or cry1/hy4 mutants, which supports the notion that COP1 actsdownstream of multiple photoreceptors (11, 113). Overexpression of COP9 re-sulted in a similar but less dramatic elongation of the hypocotyl, again most pro-nounced under blue and far-red light, although no inhibitory effect on cotyledoncell expansion could be discerned (N Wei & X-W Deng, unpublished data).Therefore, the overexpression results in general confirm the conclusion that the
LIGHT CONTROL OF SEEDLING DEVELOPMENT 235pleiotropic COP/DET/FUS gene products are repressors of photomorphogenicdevelopment.REGULATION OF COP/DET/FUS ACTIVITY BY LIGHT Limited sequence identityof COP9, COP11/FUS6, and DET1 to other eukaryotic protein sequences sub-mitted in databases suggests that they participate in a highly conserved, but asyet undefined, cellular process (24a). For COP1, sequence similarity to theRing-finger class of zinc binding proteins and the β-subunit of trimeric G pro-teins is consistent with a role as a nuclear regulator of gene expression (47). Thisalone, however, does not clarify the mechanism of light regulation. COP1 andCOP9 protein are detected in dark-grown seedlings, when the proteins are ac-tive, and also in the light-grown seedlings, when they are photomorphogenicallyinactive (112, 183). Similarly, DET1 mRNA is expressed in both dark- andlight-grown seedlings (135). Therefore, the light inactivation of DET1, COP1,and COP9 is probably not mediated by the expression level but by some othermeans of posttranslational regulation. Recent studies with COP1 and COP9point out some interesting insights. Our laboratory has shown that COP9 is asubunit of a large nuclear-localized protein complex whose apparent molecularweight can be shifted upon exposure of dark-grown seedlings to light (183).This may reflect light regulation of COP9 activity through modulation ofprotein-protein interactions in the COP9 complex. While DET1 (135) and theCOP9 complex (N Wei & X-W Deng, unpublished data) appear to have the po-tential for nuclear localization, examination of the subcellular localization of fu-sion proteins between COP1 and β-glucuronidase (GUS) reporter enzymesuggested that the nucleocytoplasmic partitioning of COP1 is regulated by lightin a cell type–dependent manner (178). In root cells, where COP1 is constitu-tively active and helps to repress chloroplast development (48), GUS-COP1 isfound in the nucleus under all light conditions. In hypocotyl cells, however,GUS-COP1 is nuclear in darkness but excluded from the nucleus under constantwhite light. Upon a switch in illumination conditions from darkness to light, theprotein slowly repartitions in the hypocotyl from a nuclear to a cytoplasmic lo-cation, and vice versa (178). Complementation of the cop1-mutant phenotypeby the GUS-COP1 transgene suggests that it is a functional substitute of COP1(our unpublished data). GUS-COP1 nucleocytoplasmic repartitioning coin-cides with light-regulated developmental redifferentiation processes, but theirinitiation clearly precedes any noticeable shift of GUS-COP1 (178). Further, thekinetics of repartitioning seem independent of the presence or absence of wild-type COP1 in the genetic background (our unpublished data). It is thereforelikely that COP1 relocalization serves to maintain a developmental commit-ment that has previously been communicated to the cell by means other thanCOP1 partitioning.
236 VON ARNIM & DENG Evidence for a role of the cytoskeleton in modulating COP1 partitioninghas been obtained following the isolation of a COP1-interacting protein, CIP1(105). The subcellular localization of CIP1 is cell type–dependent. WhileCIP1 shows a fibrous, cytoskeleton-like distribution in protoplasts derivedfrom hypocotyl and cotyledons, it is localized to discrete foci in protoplastsderived from roots. The cell type–dependent localization pattern of CIP1 mayprovide a mechanism to regulate access of COP1 to the nucleus by specificprotein-protein interactions with a cytoplasmic anchor protein (105).CONCLUSIONIn the past few years a combination of molecular genetic, biochemical, andcell biological studies has brought us remarkable progress in defining thecritical players and their specific roles in mediating the light control of seed-ling development. The basic network of signaling events seems remarkablyconserved throughout the angiosperm species examined. Therefore the focuson a model organism will prove to be continuously fruitful. How light signals perceived by distinct photoreceptors are integrated tocontrol cellular development and differentiation decisions may become a ma-jor focus in the coming years. A comprehensive understanding will not onlyreveal the players involved but also how those players interact with otherstimuli, such as hormones, to reach a precise response according to the exactlight environmental cues. In particular, many decisions in the natural environ-ment are not simply all-or-none but quantitative. Therefore, physiologicalstudies will probably play increasingly greater roles in the future work.Moreover, individual light responses vary significantly among different spe-cies. Explaining the evolutionary flexibility on the basis of conserved modulesof protein function will be a major challenge in the future. In addition, most ofthe key players identified to date seem to be present in most if not all celltypes, though each cell type produces a distinct response to a particular lightstimulus. Answers to the questions presented here will bring further insightsinto the light control of seedling development.ACKNOWLEDGMENTSWe thank Jeffrey Staub for a critical review of the manuscript and Peter Quail,Ning Wei, Steve Kay, and Hong Gil Nam for communicating unpublished re-sults. Research in this laboratory was supported by grants from the NationalScience Foundation and by the National Institutes of Health. Any Annual Review chapter, as well as any article cited in an Annual Review chapter, may be purchased from the Annual Reviews Preprints and Reprints service. 1-800-347-8007; 415-259-5017; email: firstname.lastname@example.org
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