Skip to content

Advertisement

  • Research article
  • Open Access

Cell-type specific light-mediated transcript regulation in the multicellular alga Volvox carteri

BMC Genomics201415:764

https://doi.org/10.1186/1471-2164-15-764

  • Received: 6 March 2014
  • Accepted: 3 September 2014
  • Published:

Abstract

Background

The multicellular green alga Volvox carteri makes use of none less than 13 photoreceptors, which are mostly expressed in a cell-type specific manner. This gives reason to believe that trasncriptome pattern of each cell type could change differentially in response to environmental light. Here, the cell-type specific changes of various transcripts from different pathways in response to blue, red and far-red light were analyzed.

Results

In response to different light qualities, distinct changes in transcript accumulation of genes encoding proteins involved in chlorophyll and carotenoid biosynthesis, light-harvesting complexes, circadian clock and cell cycle control were observed. Namely, blue light tends to be effective to accumulate transcripts in the somatic cells; while red light leads to accumulate transcripts predominantly in the reproductive cells. Blue light also induced marked accumulation of two components of circadian rhythms only in the somatic cells, indicating that these clock-relevant components are affected by blue light in a cell-type specific manner. Further, we show that photosynthetic associated genes are regulated distinctly among cell types by different light qualities.

Conclusion

Our results suggest that Volvox uses different sophisticated cell-type specific light signaling pathways to modulate expression of genes involved in various cellular and metabolic pathways including circadian rhythms and photosynthesis in response to environmental light.

Keywords

  • Cell types
  • Light quality
  • Gene expression
  • Photoreceptors
  • Green algae

Background

The photosynthetic organisms such as free swimming microalgae use light signals to modulate a wide variety of physiological and cellular responses including sexual life cycle, circadian clock, cellular differentiation, cell cycle, nitrogen and lipid metabolism [14]. A sophisticated light-sensing system including various photoreceptors has been developed during evolution to monitor changes in the ambient light environment (quality, quantity, direction and duration) towards adjust growth and development (reviewed in [57]). Perception of light by -some of- photoreceptors activates signal transduction cascades which lead to regulate gene expression patterns during development or in response to different light signals [8, 9]. These light-induced signal transduction pathways orchestrate the expression of downstream genes responsible for various physiological processes including circadian clock, chlorophyll and carotenoid biosynthesis [10, 11].

Four major types of photoreceptors, i.e., phototropins, cryptochromes, rhodopsisns and UV-B photoreceptors, have been identified so far in the genome of volvocine algae, a group of chlorophytes including unicellular Chlamydomonas reinhardtii (hereafter Chlamydomonas) and multicellular Volvox carteri (hereafter Volvox) (reviewed in [6]). Although in vivo functions of some of these photoreceptors have been investigated in some detail in the unicellular Chlamydomonas[3, 10, 1214], little is known about the molecular background of light reception mechanisms in the multicellular Volvox. However, the confusing maze behind individual activities of photoreceptors in the multicellular Volvox could contribute to understand the link between light and complex light-affected developmental processes such as cellular differentiation [2], which have been required for the evolutionary transition from unicellular organisms into a multicellular one [15, 16]. Volvox is one of the simplest multicellular organisms composed of only two cell types, 2000–4000 biflagellate motile, terminally differentiated somatic cells, which build a monolayer at the surface of a spheroid, and around 16 much larger immotile reproductive cells (so-called gonidia), which lie just below the somatic cell sheet; the cells are embedded in a transparent sphere of glycoprotein-rich, extracellular matrix (ECM) (Figure 1) [17, 18].
Figure 1
Figure 1

Volvox photoreceptors. Photograph of multicellualr Volvox and domain composition of its photoreceptors according to the Pfam database. Two different cell types, i.e., large dark green reproductive cells and small pale biflagellate somatic cells are located below and at the surface, respectively. Photoreceptors are categorized in three groups, i.e., somatic-, reproductive- and non-cell-specific photoreceptors, on the basis of their cell-type specific transcript levels (Additional file 2: Figure S2 and Additional file 4: Figure S3). Proteins are drawn approximately to scale. Domain abbreviations are photly. (photolyase domain), FAD (flavin adenine dinucleotide binding domain), LOV (Light-oxygen-voltage), Ser/ThrK (serine/threonine kinase), RBS (retinal binding site), RHO (rhodopsin), HisK (histidine kinase), RR (response regulator), Cycl (adenylate/guanylate cyclase domain), RCC1 (regulator of chromosome condensation).

We recently have shown that Volvox photoreceptors are expressed in a cell-type-specific manner. Eight photoreceptors, i.e., a phototropin, a plant-like cryptochrome, channelrhodopsin-1 and -2 and four histidine kinase rhodopsins, highly express in the somatic cells [6, 16, 19], while only one photoreceptor, i.e. volvoxopsin-1, has been found to predominantly express in the reproductive cells [16, 20] (Figure 1). These evidences strongly suggest that distinct cell type-specific light signaling pathways orchestrate gene expression in each cell type. Here, we investigated the cell type-specific changes in transcript accumulation of genes involved in downstream light signaling pathways. First, a diversified set of genes encoding components of light-harvesting system, carotenoid biosynthesis, tetrapyrrole biosynthesis, nitrogen metabolism, circadian clock and cell cycle were selected (Table 1). Further, we examined the light-responsive expression of these genes in each cell types after exposure to blue, red and far-red lights. The results showed that the changes in transcript level underlined distinct light signaling pathways in each cell type. Moreover, we found that some of the selected genes become rapidly upregulated after the somatic cells were exposed to blue light, whereas the same genes were induced by red light in the reproductive cells. Our results show that different light qualities lead to cell-type specific expression or repression of genes, indicating the existence of different cell type specific light signaling pathways required for physiological and developmental adaptation to environmental light.
Table 1

Candidate genes chosen for analysis of cell-type specific change of transcript accumulation under blue, red and far-red light in Volvox

Gene

Description/Function

Accession Number/Reference

Percentage of sequence identity to the homologous protein from the closely related alga Chlamydomonas

Accession number of used homolog for sequence comparison/Reference

Changes in transcript in response to light/References

LHCBM6

Chloropyll a-b binding protein of LHCII type I/a major LHCII polypeptide present in the trimeric antenna complexes of PS II

XM_002959515/[21]

93.3% identity in 253 aa overlap

EDP01611/[22]

Blue, red and far-red light/[10, 11, 23]

LHL4

Lhc-like protein Lhl4/distant relative of light-harvesting Chla/b protein

XP_002956040/[21]

64.1% identity in 284 aa overlap

BAD67138/[24]

Blue, green and red light/[25]

CHLD

Magnesium chelatase subunit D, chloroplast precursor/involved in chlorophyll biosynthesis

XP_002956151/[21]

93.3% identity in 704 aa overlap

EDP07156/[22]

White, blue and red light/[10, 26]

GSA

Glutamate-1-semialdehyde 2,1-aminomutase/key enzyme for chlorophyll synthesis

XP_002950034/[21]

92.2% identity in 464 aa overlap

Q39566/[27]

Blue, red and far-red light/[10, 11, 28]

POR

Protochlorophyllide reductase/involved in protochlorophyllide and chlorophyll biosynthesis

XP_002950278/[21]

81.1% identity in 392 aa overlap

Q39617/[29]

Blue and red light/[10]

ALAD

Delta-aminolevulinic acid dehydratase/key enzyme required for early steps in chlorophyll biosynthesis

XP_002946379/[21]

91% identity in 388 aa overlap

Q42682/[30]

White, blue and green light/[11, 28]

OEE

Oxygen evolving enhancer protein 1/part of the oxygen evolving complex of photosystem II

XP_002954867/[21]

87% identity in 291 aa overlap

P12853/[31]

White light/[11]

RB60

Disulfide isomerase RB60/part of a complex that regulates the translation of the chloroplast-encoded psbA

EFJ41881/[21]

71% identity in 532 aa overlap

AAC49896/[32]

White and red light/[33]

RB38

RNA-binding protein RB38/part of a complex that regulates the translation of the chloroplast-encoded psbA

XP_002953456/[21]

53.4% identity in 371 aa overlap

AAM76787/[34]

White, blue and red/[33]

PDS

Phytoene desaturase/key enzyme for carotenoids synthesis

XP_002948155/[21]

85.3% identity in 572 aa overlap

EDP05305/[22]

Blue and red light/[10, 11, 35]

PSY

Phytoene synthase/key enzyme involved in the first step of the carotenoids biosynthetic pathway

XP_002956783/[21]

86.3% identity in 379 aa overlap

EDO97702/[22]

White and blue light/[11, 35, 36]

CDKB1

Plant specific cyclin dependent kinase/involved in the regulation of the cell cycle

XP_002947156/[21]

95.7% identity in 322 aa overlap

EDO97594/[22]

Blue and red light/[10]

CRB1

C1 subunit of the circadian RNA-binding protein CHLAMY1/associated with the circadian clock

XP_002957962/[21]

57.9% identity in 482 aa overlap

EDP08399/[22]

Blue and red light/[10]

CRB3

C3 subunit of the circadian RNA-binding protein CHLAMY1/associated with the circadian clock

XP_002946862/[21]

85.2% identity in 392 aa overlap

EDP06114/[22]

Blue and red light/[10]

ACDA

Guanylyl and adenylate cyclase family member/cAMP or cGMP production

ABM47321/[37]

63.6% identity in 154 aa overlap

XP_001702503/[22]

---------------

CA

Carbonic anhydrase/key enzyme involves in involved in carbon metabolism

XP_002951242/[21]

50.8% identity in 374 aa overlap

BAA14232/[38]

White, blue and red light/[36, 39]

GLN1

Glutamine synthetase/key enzyme in nitrogen metabolism

XP_002956198/[21]

92.1% identity in 382 aa overlap

U46207/[40]

White, blue and red light/[10, 40]

FBP

Fructose-1,6-bisphosphatase/key enzymes involved in gluconeogenesis and the Calvin cycle

XP_002948170 [21]

88% identity in 415 aa overlap

XP_001690872/[22]

White light/[36]

RPE

Ribulose phosphate-3-epimerase/key enzymes involved in the Calvin cycle

Photozyme ID: Vocar20000806m.g/[21]

90.2% identity in 264 aa overlap

XP_001691071/[22]

White light/[36]

Methods

Strain and culture conditions

Cultures of Volvox carteri f. nagariensis female strain Eve10 [41] were maintained in standard Volvox medium [42] at 28°C in a cycle of 8 h dark/16 h cool fluorescent white light at an average of ~100 μmol photons m-2 s-1 photosynthetically-active radiation (PAR). The reproductive and somatic cells were separated three hours before initiation of cleavage division (Additional file 1: Figure S1A) using Dounce homogenizer as described previously [37].

Light treatments

To analyze cell-type specific light-mediated gene expression, the isolated reproductive and somatic cells were incubated for 26 hours in the dark before exposure to the test light of specific wavelengths for 1 hour (Additional file 1: Figure S1B). Light treatments were performed using LEDs of specific wavelengths with following equipment and settings: for blue light, Luxeon Rebel High Power Blue LED (Philips Lumileds), peak at 470 nm (with a typical spectral half-width of 20 nm) and a photon fluence rate of 15 μmol photons m-2 s-1; for red light, Luxeon Rebel High Power Deep Red LED (Philips Lumileds), peak at 655 nm (with a typical spectral half-width of 20 nm) and a photon fluence rate of 15 μmol photons m-2 s-1; for far-red light, High Efficacy Far Red LED (LED Engin), peak at 735 nm (with a typical spectral half-width of 25 nm) and a photon fluence rate of 15 μmol photons m-2 s-1 (Additional file 2: Figure S2). The light fluence rates were measured using a LI-250A light meter (Li-COR) and a red light meter (Model 9.6 Visible Red Light Meter, Solartech inc.).

RNA isolation

Total RNA was extracted from all samples using TRI Reagent (Sigma-Aldrich, St. Louis, MO) as described previously [19]. The extracted RNA was dissolved in RNase-free water and stored at -70°C. The integrity and size distribution of total RNA was checked by denaturing agarose-formaldehyde gel electrophoresis. The quantity and quality of extracted RNA were determined spectrophotometrically using an Ultrospec 2100 proUV/Visible Spectrophotometer (GE Healthcare) at 260 and 280 nm.

Quantitative one-step real-time RT-PCR and data analysis

Primers were designed to amplify cDNA fragments with 109 to 144 bp in length (Additional file 3: Table S1). 1 μg total RNA from each cell type (dark-adapted and after light treatments) was treated with 5 units DNaseI (Promega, Madison, WI) in DNase-I buffer (20 mM Tris, pH 8.4, 2 mM MgCl2, 50 mM KCl) in a total volume of 10 μl at 37°C for 10 min to remove contaminating DNA within the RNA preparation. The reaction was stopped by the addition of 1 μl 25 mM EDTA and incubation at 65°C for 10 min. The RNA concentration was measured before and after DNAse-I treatment to ensure that the same RNA amount from different cell types were used in all reactions. The real-time RT-PCR was performed on a CFX96TM real-time PCR detection system (Bio-Rad) using the SensiFAST SYBR One-Step Kit (Bioline). All reactions contained 300 ng DNase-I-treated template RNA in a total volume of 20 μl. The reactions were incubated for 30 min at 50°C for cDNA synthesis followed by 2 min incubation at 95°C for initial Tag polymerase activation. The reactions were then subjected to 40 cycles of amplification, which consisted of a denaturing step at 95°C for 5 s, an annealing step at 57°C for 10 s and an extension step at 72°C for 5 s. All real-time RT-PCR experiments were carried out in triplicate from two different biological samples together with controls lacking RT or template to detect potential DNA contaminations. The relative expression level has been calculated using the 2-∆∆Ct as described previously [37, 43]. RACK1, which has previously been used for normalization of light-dependent gene expression in the closely related algae Chlamydomonas reinhardtii[10, 11] and shows constitutive expression in both reproductive and somatic cells, was used for normalization of cell type specific light-mediated gene expression data.

Results

Reproductive and somatic cells accumulate different photoreceptors

The study of Volvox photoreceptors was almost always accompanied by questions regarding their cell-type specific functions. This multicellular green alga makes use of no less than 13 photoreceptors, i.e., seven rhodopsin-like photoreceptors (VR1, VChR1, VChR2, VcHKR1, VcHKR2, VcHKR3 and VcHKR4), one UV-B photoreceptor (VcUVR8), four crypochromes (VcCRYa, VcCRYp, VcCRYd1 and VcCRYd2) and one phototropin (VcPhot) (Figure 1). In addition to the previous studies which showed that VR1 and channelrhodopsins are highly expressed in the reproductive and somatic cells, respectively [19, 20], recent investigations revealed that most photoreceptors are expressed in a cell-type specific manner [6, 16] (Figure 1). These observations raise the question about the existence of different cell-type specific light signaling pathways in Volvox. To address this issue, we analyzed the cell-type specific change in the transcript accumulation of a set of genes which show light-induced changes in gene expression and are parts of downstream light signaling pathways [10, 11, 23, 25, 33, 35, 36, 39]. For this purpose, the reproductive and somatic cells were separated three hours before initiation of cleavage division, followed by 26 h of incubation in the dark before exposure to blue, red or far-red light (Additional file 1: Figure S1A-B). However, because the cell-type specific transcript level of photoreceptors depends on the developmental stages, we analyzed their transcript levels right after separation of cell types, i.e. three hours before initiation of cleavage division, and at the end of dark incubation step (Additional file 1: Figure S1A-B). The results were in accordance with the previously reported data [6, 16, 19, 20] and showed the same localization of cellular expression for Volvox photoreceptors (Additional file 4: Figure S3 and Additional file 5: Figure S4, Figure 1).

Volvoxgenes encoding components of light-harvesting system, carotenoid and chlorophyll biosynthesis, circadian clock, cell cycle and diverse metabolic pathways

In order to examine whether distinct cell-type specific light signaling pathways are exist in Volvox, the impact of light quality on the expression of a variety of genes encoding components of light-harvesting system, carotenoid and chlorophyll biosynthesis, circadian clock, cell cycle and diverse metabolic pathways was investigated. Because of the absence of any report studying light-mediated gene expression in Volvox, candidate genes were selected based on available observations from other algal systems such as Chlamydomonas and Phaeodactylum tricornutum[10, 11, 26, 33, 35, 36]. The genes encoding components involved in light-harvesting system and chlorophyll biosynthesis include chloropyll a-b binding protein of LHCII type I (LHCBM6), a distant relative of light-harvesting chloropyll a-b protein (LHL4), magnesium chelatase subunit D (CHLD), glutamate-1-semialdehyde 2,1-aminomutase (GSA), protochlorophyllide reductase (POR), delta-aminolevulinic acid dehydratase (ALAD), oxygen evolving enhancer protein 1 (OEE), disulfide isomerase RB60 (RB60) and RNA-binding protein RB38 (RB38) (Table 1). Two genes encoding enzymes of carotenoid biosynthesis pathway, i.e., phytoene desaturase (PDS) and phytoene synthase (PSY), that have been shown to be controlled by light [10, 11, 35, 36] were also selected. Additional genes encoding clock and cell cycle relevant components including C1 and C3 subunits of the circadian RNA-binding protein CHLAMY1 (CRB1 and CRB3) and a plant specific cyclin dependent kinase (CDKB1) were also analyzed (Table 1). Furthermore, genes encoding proteins involved in nitrogen metabolism (GLN1), carbon metabolisms (CA and FBP), pentose phosphate pathway (PRE) and a guanylyl and adenylate cyclase family member (Table 1) have been added to this study. None of these genes had been studied before in Volvox concerning blue, red and far-red light-dependent regulation.

Cell-type specific changes in transcript accumulation of genes encoding photosynthetic related/associated components in response to blue and red light

In plants including algae, red and blue light have been shown to regulate the expression of photosynthetic associated genes [25, 44, 45]. To examine the effect of blue and red light on cell-type specific transcript accumulation of genes encode components of photosynthetic apparatus and related regulatory elements in Volvox, the reproductive and somatic cells were exposed to the monochromic blue (470 nm) and red (655 nm) light of equal photon fluence rate of 15 photons m-2 s-1 for 1 h (Additional file 1: Figure S1). As shown in Figure 2, the transcript levels of LHL4 and CHLD increased in response to blue light in both cell types (Figure 2A), while red light led to a marked increase in LHL4 transcript (~11-fold) only in the somatic cells (Figure 2B). Following exposure of cell types to the blue light, the transcript of LHCBM6 increased in the somatic cells, but remained unchanged in the reproductive cells (Figure 2A). In contrast, slightly elevated transcript level of LHCBM6 was only observed in the reproductive cells in response to red light (Figure 2B). Furthermore, the level of POR transcript increased in response to the blue light in the somatic cells and, remarkably, decreased in those cells after exposure to the red light. However, only red light could elicit elevated expression of POR transcript in the reproductive cells (Figure 2A-B). Moreover, the transcript level of OEE increased in response to the red light in the reproductive cells, whereas blue light led to decrease its level in these cells. The detected changes in the transcript level of OEE in the somatic cells seem to be not statistically significant. The transcript of RB60 increased in the somatic (remarkably) and reproductive (moderately) cells following blue light treatment, while red light led to elevated transcript level only in the reproductive cells (Figure 2A-B). These results show that blue and red light regulate the expression of genes encoding photosynthetic relevant components in both cell types in different ways, suggesting that cell-type specific light-induced signal transduction pathways underlying light-induced changes of photosynthetic related transcripts.
Figure 2
Figure 2

Blue and red light-induced changes in transcript accumulation of genes encoding photosynthesis components. The reproductive and somatic cells from vegetative algae were separated 3 h before initiation of cleavage divisions and incubated for 26 h in the dark before exposure to blue (A, 470 nm; 15 μmol photons m-2 s-1) and red (B, 655 nm; 15 μmol photons m-2 s-1) light for 1 hour (Additional file 1: Figure S1A-B). The transcript levels were calculated using the 2-∆∆Ct method and RACK1 as reference gene. Each experiment was performed in triplicate from at least two different biological samples. The data were averaged and statistically treated (t-test, *P < 0.05; **P < 0.01). Bars show means and standard deviations.

Blue and red light-induced changes in transcript accumulation of genes encoding carotenoid biosynthesis, cell cycle and clock relevant components in the reproductive and somatic cells

In the closely related alga Chlamydomonas, expression of two genes involved in carotenoids biosynthesis pathway, PDS and PSY, is affected by blue and red light [10, 11, 35]. In the multicellular Volvox, the transcript of PDS accumulated in each cell type in response to different light quality. Whereas blue light led to increase the transcript level of PDS in the somatic cells, red light induced accumulation of this transcript in the reproductive cells (Figure 3A-B). Unlike PDS, PSY transcript increased in both cell types after blue light irradiation. Red light, however, induced accumulation of PSY transcript only in the reproductive cells (Figure 3A-B). We also analyzed the effect of blue and red light on the transcript levels of two subunits of the circadian RNA-binding protein CHLAMY1, i.e., CRB1 and CRB2, which are shown to be associated with circadian clock in green algae [46]. A marked increase in transcript level of CRB3 (~20-fold) was observed in the somatic cells after exposure to blue light (Figure 3A). CRB1 also exhibited a relatively high transcript accumulation in these cells following blue light exposure (Figure 3A). In the reproductive cells, however, the transcript level of CRB1 and CRB3 were increased moderately in response to blue light. Remarkably, no significant changes in transcript level of these genes have been observed when the somatic cells were exposed to red light (Figure 3B). But in contrast, red light led to modest change in the transcript level of CBR1 and CRB3 in the reproductive cells (Figure 3A-B).
Figure 3
Figure 3

Blue and red light-induced changes in transcript accumulation of genes encoding cell cycle, clock and carotenoid biosynthesis components. Cell type separation and light treatments using blue (A, 470 nm; 15 μmol photons m-2 s-1) and red (B, 655 nm; 15 μmol photons m-2 s-1) light were done as described in Figure 2 and Additional file 1: Figure S1A-B. Each experiment was performed in triplicate from at least two different biological samples. The data were averaged and statistically treated (t-test, *P < 0.05; **P < 0.01). Bars show means and standard deviations.

Recently, it was shown that the transcript level of CDKB1, a plant specific cyclin-dependent kinase which is involved in the regulation of the cell cycle [47, 48], gradually increases following exposure of dark-adapted Chlamydomonas cells to red light. However, only modest changes in transcript abundance were observed after irradiation with blue light [10]. In Volvox, blue light elevated the transcript level of CDKB1 only in the somatic cells (Figure 3A). Moreover, a small elevation in the transcript level of CDKB1 in the reproductive cells was observed following exposure to red light, while no significant change has been observed in the somatic cells (Figure 3B). These results indicated that blue light induces transcript accumulation of the genes involved in circadian clock and cell cycle in the somatic cells, whereas no blue light-induced changes were observed in the reproductive cells.

Blue and red light induced modulation of ACDA and CAtranscript abundance

Class III guanylyl and adenylyl cyclases represent one of the largest known protein families in the genome of Chlamydomonas and Volvox[21, 22]. Although these cyclases are not identified so far in plants, they catalyze the synthesis of cGMP and cAMP, which serve as second messengers in a variety of signaling processes, in animals, fungi and prokaryotes [49, 50]. A member of the guanylyl and adenylate cyclase family, i.e., ACDA, which has been previously shown to be more expressed in the somatic cells than in reproductive ones [37], was analyzed here. In the somatic cells, blue light led to induce expression of ACDA, however, the level was remarkably reduced (~5-fold) following exposure of the cells to the red light (Figure 4A-B). Both blue and red light caused also decreased level of CA transcript encoding a zinc-containing carbonic anhydrase in the somatic cells. In contrast, the level of ACDA and CA transcripts was increased in response to the red light in the reproductive cells (Figure 4A-B).
Figure 4
Figure 4

Blue and red light-induced changes in transcript accumulation of genes encoding components of diverse metabolic pathways. Cell types were separated as described in Figure 2 and Additional file 1: Figure S1A. After 26 h of dark incubation, the cells were exposed to blue (A, 470 nm; 15 μmol photons m-2 s-1) and red (B, 655 nm; 15 μmol photons m-2 s-1) light for 1 h. Each experiment was performed in triplicate from at least two different biological samples. The data were averaged and statistically treated (t-test, *P < 0.05; **P < 0.01). Bars show means and standard deviations.

Far-red light causes only modest changes in the levels of transcripts from LHL4, PSY and ACDA

Plants make use of red/far-red light-absorbing phytochrome photoreceptors to measure the ratio of red/far-red light that mediate physiological responses by regulating gene expression [51, 52]. Although phytochromes also have been found in charophyta, a division of green algae that includes the closest relatives of the embryophyte plants [53, 54]; no phytochrome genes could be identified in the genomes of volvocine algae Volvox and Chlamydomonas, even though red- and far-red-regulated gene expression has been observed [6, 10, 11, 33]. As shown in Additional file 6: Figure S5, we could only detect the modest effect of far-red light (735 nm, photon fluence rate of 15 photons m-2 s-1) on the transcript levels of LHL4, PSY and ACDA. Whereas the transcript level of LHL4 and PSY increased in the somatic cells after far-red light treatments, a reduced level of ACDA transcript was observed in both cell types (Additional file 6: Figure S5). These results indicate that the changes in transcript level of genes analyzed in this study are more sensitive to the blue and red light than far-red light. On the other hand, this observation could be interpreted as small support for the existence of a putative far-red-light signaling pathways in the volvocine algae including Volvox.

Discussion

In this study, cell-type specific changes of transcript accumulation of genes associated with various metabolic and cellular pathways in response to the light of different wavelengths were analyzed in Volvox. With respect to the cell-type specific photoreceptors, it is very likely that this multicellular alga uses different cell-type specific light signaling pathways to regulate gene expression in a cell-type specific fashion. The results presented here provide an insight into the cell-types specific changes of transcript accumulation which is required to utilize environmental clues such as light towards adequate adaptation of light-affected cellular and developmental processes in each cell type.

Blue and red light induce quantitative difference of transcript accumulation in both cell types

Plants including algae use various kinds of photoreceptors to sense changes in environmental light and to mediate diverse physiological and developmental processes by photoreceptor-mediated orchestrating of gene expression [52, 55]. These light-sensitive proteins allow efficient reprogramming of transcriptome by light-induced activation of transcription factors or regulation of light-induced splicing of target genes [56, 57]. Moreover, tissue or developmentally regulated expression of photoreceptors and/or associated signaling components triggers changes in transcript level of distinct target genes in different organs [5860]. Considering the fact that the most Volvox photoreceptors are expressed in a cell-type specific manner (Figure 1), the main issue to be dealt with is whether this multicellular alga makes use of different distinct light signaling pathways to regulate gene expression in its two entirely different cell types, especially in response to the environmental light. The data presented here show that blue and red light induce cell-type specific changes in the level of transcripts from the most but not all analyzed genes. The transcript of four genes belonging to various functional categories, i.e., POR, PDS, CRB1 and ACDA, accumulated in the reproductive and somatic cells in response to different light qualities, i.e., red and blue light, respectively (Figure 5). Our data also show that the transcript accumulation in the somatic cells is more sensitive to blue light (14 genes), while red light led to accumulate more transcripts (15 genes) in the reproductive cells (Figure 5). Only GLN1 and LHL4 showed increase in transcript levels after red light treatment in the somatic cells. In the closely related alga Chlamydomonas, blue light was shown to be more effective for inducing LHL4 gene expression than red or far-red light [25]. However, although LHL4 transcript accumulated in both Volvox cell types in response to blue light (Figure 2A), red (a marked increase) and far-red (a modest increase) light could elicit elevated expression only in the somatic cells (Figure 2B, Figure 5 and Additional file 6: Figure S5).
Figure 5
Figure 5

Cell-type specific light-mediated changes of transcript level. Enhanced gene expression by blue (470 nm) and red (655 nm) light in the somatic (S) and reproductive (R) cells is highlighted by blue and red, respectively, while repressed expression is shown by black. Grey shows no change in transcript level under given light-treatment. * and ** indicate more than four- and eight-fold increase in transcript level, respectively.

In higher plants, a large number of genes are obviously repressed by blue, red and far-red light [9, 61, 62]. Among analyzed genes in this study, only five transcripts were found to be repressed (with a ratio of 0.31-fold or less) in the somatic cells after 1 h of blue and/or red light irradiation; the carbonic anhydrase gene CA was down regulated following both blue and red light treatments (Figure 4A-B), while ACDA, GSA, PRE and POR were decreased only in response to red light (Figure 2B and Figure 4B). On the other hand, in the reproductive cells, the transcripts of all these five genes were increased after red light treatment (Figure 5). This indicates that the same light quality causes induction or repression of genes in a cell type-dependent fashion, suggesting that different transcription factors could be involved in downstream red-light-signaling pathway in the two cell types.

Cell-type specific light signaling pathways behind cellular differentiation

During evolution, the development of complex eukaryotic organisms such as Volvox is generated through selective expression of specific fraction of the same genome in different cell types in response to developmental and environmental cues [59, 63]. The two cell types of this multicellular alga represent differential expression pattern of genes from various functional classes [37, 64, 65]. However, little is known regarding cell-type specific changes of gene expression in response to environmental cues including light, which is one of most important environmental signals for controlling growth and development in plants including algae [1, 5, 6, 66, 67]. In plants, for example, blue and red/far-red light are of great importance for the optimization of cellular and developmental processes such as photosynthesis by shade avoidance response and chloroplast positioning [44, 6870]. Moreover, it is generally assumed that photoreceptors induce light-modulated gene expression to direct appropriate growth and developmental responses [44, 62, 71]. Comparison of the gene expression profiles of the reproductive and somatic cells reported here revealed that distinct cell-type specific light signaling pathways underlying gene expression modulate appropriate transcript regulation in response to light. Thus, different qualities of light appear to trigger distinct cell-type specific changes in transcript level (Figure 5). In particular, blue light increased the transcript level of two photosynthetic relevant components, i.e., LHCBM6 and POR, only in the somatic cells, while those levels were elevated in the reproductive cells by red light (Figure 2A-B). On the other hand, a marked increase in LHL4 transcript was observed in the somatic cells exposure to red light, while no change was detected in the reproductive cells exposure to the same light quality (Figure 2B). In Volvox, regulation of photosynthesis is believed to be the key difference between both cell types. Whereas nuclear genes encode important chloroplast proteins are expressed abundantly in the reproductive cells, repression of their transcription in the somatic cells blocks reproductive activity by preventing cell growth [65, 72, 73]. In Chlamydomonas, expression of genes associated with photosynthetic function is affected by blue and red light [23, 25, 33]. Light signaling mediated by phototropin and cryptochrome was shown to be implicated in the induction of gene expression [10, 11]. The observed cell-type specific changes in transcript accumulation of genes associated with photosynthesis in response to light can be traced back to the Volvox photoreceptors, which are mostly expressed in a cell-type specific fashion.

In addition, we observed that the transcript of CRB1 and CRB3 genes encoding C1 and C3 subunits of RNA-binding protein CHLAMY1, respectively, increased in response to blue light in the somatic cells, but not in the reproductive cells. It has previously been reported that the binding activity of CHLAMY1 changes in a circadian manner [74]. Interaction between CHLAMY1 and these subunits is necessary for RNA-binding activity [75]. Moreover, changes in the level of C1 and C3 affect circadian rhythms in Chlamydomonas[46]. A marked increase in the transcript of CRB3 in the somatic cells after 1 h exposure to blue light (~20-fold) is also consistent with recent report by Beel et al.[10] that showed an ~15-fold increase in the C3 transcript after the cells were exposed to 30 min of blue light [10]. However, in contrast, we did not observed any effect of red and far-red light on the transcript level of CRB3 and CRB1 in the somatic cells, indicating that blue light is more effective for inducing these clock-relevant components. Therefore, based on these observations in conjunction with a previous study by Iliev et al.[46], it is logical to suggest that blue light affect circadian rhythms in a cell-type specific manner. This conclusion is consistent with a recently reported study about cell-type specific circadian rhythms in Arabidopsis, which demonstrated that stomatal guard cells have a different period from surrounding epidermal and mesophyll leaf cells [76].

Biological significance of cell-type specific light signaling pathways

In nature, the Volvox populations swim downward to reach cool and dark regions at twilight and then swim back to the euphotic zone at dawn [77]. Because of the wavelength dependent penetration of the light in water [78, 79], changes in detected wavelengths or spectral composition of light could be detected as an environmental signal cue to swim down- or upward at twilight and dawn, respectively, and to regulate developmental and physiological processes for day and night adaptation. Obviously, Volvox makes use of a variety of photoreceptors to sense changes in light properties (direction, quality and intensity). Diverse photoreceptors have been shown to be localized within the eyespot of volvocine algae [19, 80, 81], indicating that eyespot and associated structures [5] serve as general sensory organelles to modulate photobehavior, i.e., phototaxis and photophobic responses, and potentially other developmental or adaptive responses. Thus, the eyespot apparatus is required for accurate light-monitoring and light-dependent movement responses to optimize the photosynthetic activities or to avoid photodamages. In Volvox, eyespots are exclusively restricted to the somatic cells, in which the most photoreceptor genes are expressed. On other hand, only VR1 is highly expressed in the reproductive cells (Figure 1). Cell-type specific distribution of photoreceptors enables both cell types to optimize cellular and developmental processes differentially in response to environmental light. In addition, light also serves as a time cue that daily resets the circadian rhythms. The light quality, e.g., amount and spectral composition, changes during twilight. For example, twilight is primarily characterized by relative enrichment of the shorter wavelengths (<500 nm) compared to the mid-long wavelengths (500–650 nm) [82]. The ability to sense changes in the light quality (for example, detection of blue light at dawn) triggers signaling pathways towards adjusting cellular processes. However, the marked changes in transcripts of clock relevant components CRB1 and CRB3 in the somatic cells in response to only blue light indicate that each cell type has its own genetically predefined circadian rhythm. Moreover, depends on environmental light, physiological and metabolic activities have been shown to be fine-tuned in green algae (reviewed in [1]). In Chlamydomonas, it was shown that the activity of carbonic anhydrase (CA) is under blue and red light control. The authors could show that photosynthesis is required for regulation of CA and, in addition, a blue light stimulated mechanism is also involved in CA transcript regulation [39]. Moreover, inhibition studies and mutant analysis have shown that CA is important to the function of photosynthesis in Chlamydomonas[83]. In Volvox, photosynthetic activities seem to be differentially regulated, in the light of morphological and physiological differences between two cell types. Illumination of reproductive cells with red light (which is needed for the photosynthesis-dependent process) led to accumulation of CA transcript, while both blue and red light led to reduce its transcript level in the somatic cells (Figure 4). In other words, depending on cell type, light signals could increase or decrease photosynthetic activities. Therefore, it is to assume that distinct light signaling pathways have been evolved to modulate differential regulation of photosynthetic related components in response to environmental light that ensure development and function of specific types of cells.

Conclusions

The results presented here demonstrate that the multicellular green alga Volvox uses different cell-type specific light signaling pathways to modulate gene expression in a cell-type specific manner. This sophisticated gene expression system has been potentially assured through cell-type specific expression of photoreceptors and allows differential regulation of genes involved in various cellular and metabolic pathways in response to environmental light.

Availability of supporting data

The data sets supporting the results of this article are included within the article and its additional files.

Declarations

Acknowledgements

I thank Noriko Ueki (Department of Biological Sciences, Chuo University) for reading of the manuscript and helpful suggestions. I also would like to gratefully thank Kordula Puls for technical assistance and Achim Müller for constructing LEDs and electronic devices required for light-dependent gene expression analysis in this study. I also wish to thank Prof. Dr. Armin Hallmann for the possibility to conduct all experiments in his lab. This work was funded by a grant (KI 1779/1-1) from the German Research Foundation (DFG) to AK.

Authors’ Affiliations

(1)
Department of Cellular and Developmental Biology of Plants, , University of Bielefeld, Universitätsstr. 25, D-33615 Bielefeld, Germany

References

  1. Grossman AR, Lohr M, Im CS: Chlamydomonas reinhardtii in the landscape of pigments. Annu Rev Genet. 2004, 38: 119-173.PubMedView ArticleGoogle Scholar
  2. Kirk MM, Kirk DL: Translational regulation of protein-synthesis, in response to light, at a critical stage of Volvox development. Cell. 1985, 41 (2): 419-428.PubMedView ArticleGoogle Scholar
  3. Huang KY, Beck CF: Photoropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 2003, 100 (10): 6269-6274.PubMed CentralPubMedView ArticleGoogle Scholar
  4. Oldenhof H, Zachleder V, van den Ende H: Blue light delays commitment to cell division in Chlamydomonas reinhardtii. Plant Biol (Stuttg). 2004, 6 (6): 689-695.View ArticleGoogle Scholar
  5. Foster KW, Smyth RD: Light antennas in phototactic algae. Microbiol Rev. 1980, 44 (4): 572-630.PubMed CentralPubMedGoogle Scholar
  6. Kianianmomeni A, Hallmann A: Algal photoreceptors: in vivo functions and potential applications. Planta. 2014, 239 (1): 1-26.PubMedView ArticleGoogle Scholar
  7. Hegemann P: Algal sensory photoreceptors. Annu Rev Plant Biol. 2008, 59: 167-189.PubMedView ArticleGoogle Scholar
  8. Liu B, Zuo ZC, Liu HT, Liu XM, Lin CT: Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev. 2011, 25 (10): 1029-1034.PubMed CentralPubMedView ArticleGoogle Scholar
  9. Jiao Y, Yang H, Ma L, Sun N, Yu H, Liu T, Gao Y, Gu H, Chen Z, Wada M, Gerstein M, Zhao H, Qu LJ, Deng XW: A genome-wide analysis of blue-light regulation of Arabidopsis transcription factor gene expression during seedling development. Plant Physiol. 2003, 133 (4): 1480-1493.PubMed CentralPubMedView ArticleGoogle Scholar
  10. Beel B, Prager K, Spexard M, Sasso S, Weiss D, Muller N, Heinnickel M, Dewez D, Ikoma D, Grossman AR, Kottke T, Mittag M: A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell. 2012, 24 (7): 2992-3008.PubMed CentralPubMedView ArticleGoogle Scholar
  11. Im CS, Eberhard S, Huang K, Beck CF, Grossman AR: Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. Plant J. 2006, 48 (1): 1-16.PubMedView ArticleGoogle Scholar
  12. Sineshchekov OA, Jung KH, Spudich JL: Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 2002, 99 (13): 8689-8694.PubMed CentralPubMedView ArticleGoogle Scholar
  13. Deininger W, Kroger P, Hegemann U, Lottspeich F, Hegemann P: Chlamyrhodopsin represents a new type of sensory photoreceptor. EMBO J. 1995, 14 (23): 5849-5858.PubMed CentralPubMedGoogle Scholar
  14. Trippens J, Greiner A, Schellwat J, Neukam M, Rottmann T, Lu Y, Kateriya S, Hegemann P, Kreimer G: Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii. Plant Cell. 2012, 24: 4687-4702.PubMed CentralPubMedView ArticleGoogle Scholar
  15. Kirk DL: A twelve-step program for evolving multicellularity and a division of labor. Bioessays. 2005, 27 (3): 299-310.PubMedView ArticleGoogle Scholar
  16. Kianianmomeni A, Hallmann A: Transcriptional analysis of Volvox photoreceptors suggests the existence of different cell-type specific light signaling pathways. Curr Genet. 2014, doi:10.1007/s00294-014-0440-3Google Scholar
  17. Kirk D: Volvox: molecular-genetic origins of multicellularity and cellular differentiation. 1998, Cambridge, UK: Cambridge University PressGoogle Scholar
  18. Hallmann A: Extracellular matrix and sex-inducing pheromone in Volvox. Int Rev Cytol. 2003, 227: 131-182.PubMedView ArticleGoogle Scholar
  19. Kianianmomeni A, Stehfest K, Nematollahi G, Hegemann P, Hallmann A: Channelrhodopsins of Volvox carteri are photochromic proteins that are specifically expressed in somatic cells under control of light, temperature, and the sex inducer. Plant Physiol. 2009, 151 (1): 347-366.PubMed CentralPubMedView ArticleGoogle Scholar
  20. Ebnet E, Fischer M, Deininger W, Hegemann P: Volvoxrhodopsin, a light-regulated sensory photoreceptor of the spheroidal green alga Volvox carteri. Plant Cell. 1999, 11 (8): 1473-1484.PubMed CentralPubMedView ArticleGoogle Scholar
  21. Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS: Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science. 2010, 329 (5988): 223-226.PubMed CentralPubMedView ArticleGoogle Scholar
  22. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, et al: The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science. 2007, 318 (5848): 245-250.PubMed CentralPubMedView ArticleGoogle Scholar
  23. Johanningmeier U, Howell SH: Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardi. Possible involvement of chlorophyll synthesis precursors. J Biol Chem. 1984, 259 (21): 13541-13549.PubMedGoogle Scholar
  24. Teramoto H, Itoh T, Ono TA: High-intensity-light-dependent and transient expression of new genes encoding distant relatives of light-harvesting chlorophyll-a/b proteins in Chlamydomonas reinhardtii. Plant Cell Physiol. 2004, 45 (9): 1221-1232.PubMedView ArticleGoogle Scholar
  25. Teramoto H, Ishii A, Kimura Y, Hasegawa K, Nakazawa S, Nakamura T, Higashi S, Watanabe M, Ono TA: Action spectrum for expression of the high intensity light-inducible Lhc-like gene Lhl4 in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol. 2006, 47 (3): 419-425.PubMedView ArticleGoogle Scholar
  26. Vasileuskaya Z, Oster U, Beck CF: Involvement of tetrapyrroles in inter-organellar signaling in plants and algae. Photosynth Res. 2004, 82 (3): 289-299.PubMedView ArticleGoogle Scholar
  27. Matters GL, Beale SI: Structure and light-regulated expression of the gsa gene encoding the chlorophyll biosynthetic enzyme, glutamate 1-semialdehyde aminotransferase, in Chlamydomonas reinhardtii. Plant Mol Biol. 1994, 24 (4): 617-629.PubMedView ArticleGoogle Scholar
  28. Matters GL, Beale SI: Blue-light-regulated expression of genes for two early steps of chlorophyll biosynthesis in Chlamydomonas reinhardtii. Plant Physiol. 1995, 109 (2): 471-479.PubMed CentralPubMedGoogle Scholar
  29. Li J, Timko MP: The pc-1 phenotype of Chlamydomonas reinhardtii results from a deletion mutation in the nuclear gene for NADPH:protochlorophyllide oxidoreductase. Plant Mol Biol. 1996, 30 (1): 15-37.PubMedView ArticleGoogle Scholar
  30. Matters GL, Beale SI: Structure and expression of the Chlamydomonas reinhardtii alad gene encoding the chlorophyll biosynthetic enzyme, delta-aminolevulinic acid dehydratase (porphobilinogen synthase). Plant Mol Biol. 1995, 27 (3): 607-617.PubMedView ArticleGoogle Scholar
  31. Mayfield SP, Schirmerrahire M, Frank G, Zuber H, Rochaix JD: Analysis of the genes of the OEE1 and OEE3 proteins of the photosystem II complex from Chlamydomonas reinhardtii. Plant Mol Biol. 1989, 12 (6): 683-693.PubMedView ArticleGoogle Scholar
  32. Kim JM, Mayfield SP: Protein disulfide isomerase as a regulator of chloroplast translational activation. Science. 1997, 278 (5345): 1954-1957.PubMedView ArticleGoogle Scholar
  33. Alizadeh D, Cohen A: Red light and calmodulin regulate the expression of the psbA binding protein genes in Chlamydomonas reinhardtii. Plant Cell Physiol. 2010, 51 (2): 312-322.PubMed CentralPubMedView ArticleGoogle Scholar
  34. Barnes D, Cohen A, Bruick RK, Kantardjieff K, Fowler S, Efuet E, Mayfield SP: Identification and characterization of a novel RNA binding protein that associates with the 5′-untranslated region of the chloroplast psbA mRNA. Biochemistry. 2004, 43 (26): 8541-8550.PubMedView ArticleGoogle Scholar
  35. Bohne F, Linden H: Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinhardtii. Biochim Biophys Acta. 2002, 1579 (1): 26-34.PubMedView ArticleGoogle Scholar
  36. Coesel S, Mangogna M, Ishikawa T, Heijde M, Rogato A, Finazzi G, Todo T, Bowler C, Falciatore A: Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO Rep. 2009, 10 (6): 655-661.PubMed CentralPubMedView ArticleGoogle Scholar
  37. Nematollahi G, Kianianmomeni A, Hallmann A: Quantitative analysis of cell-type specific gene expression in the green alga Volvox carteri. BMC Genomics. 2006, 7: 321-PubMed CentralPubMedView ArticleGoogle Scholar
  38. Fukuzawa H, Fujiwara S, Tachiki A, Miyachi S: Nucleotide sequences of two genes CAH1 and CAH2 which encode carbonic anhydrase polypeptides in Chlamydomonas reinhardtii. Nucleic Acids Res. 1990, 18 (21): 6441-6442.PubMed CentralPubMedView ArticleGoogle Scholar
  39. Dionisio-Sese ML, Fukuzawa H, Miyachi S: Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol. 1990, 94 (3): 1103-1110.PubMed CentralPubMedView ArticleGoogle Scholar
  40. Chen Q, Silflow CD: Isolation and characterization of glutamine synthetase genes in Chlamydomonas reinhardtii. Plant Physiol. 1996, 112 (3): 987-996.PubMed CentralPubMedView ArticleGoogle Scholar
  41. Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, Kirk DL: Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet. 1990, 18 (2): 141-153.PubMedView ArticleGoogle Scholar
  42. Provasoli L, Pintner IJ: Artificial Media for Fresh-Water Algae: Problems and Suggestions. The Ecology of Algae, a Symposium Held at the Pymatuning Laboratory of Field Biology on June 18 and 19, 1959, (ed). Edited by: Tryon CA, Hartman RT. 1959, Pittsburgh, PA: The Pymatuning Symposia in Ecology, Special Publication No 2, University of Pittsburgh, 84-96.Google Scholar
  43. Kianianmomeni A, Hallmann A: Validation of reference genes for quantitative gene expression studies in Volvox carteri using real-time RT-PCR. Mol Biol Rep. 2013, 40: 6691-6699.PubMedView ArticleGoogle Scholar
  44. Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW: Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell. 2001, 13 (12): 2589-2607.PubMed CentralPubMedView ArticleGoogle Scholar
  45. Hamazato F, Shinomura T, Hanzawa H, Chory J, Furuya M: Fluence and wavelength requirements for Arabidopsis CAB gene induction by different phytochromes. Plant Physiol. 1997, 115 (4): 1533-1540.PubMed CentralPubMedView ArticleGoogle Scholar
  46. Iliev D, Voytsekh O, Schmidt EM, Fiedler M, Nykytenko A, Mittag M: A heteromeric RNA-binding protein is involved in maintaining acrophase and period of the circadian clock. Plant Physiol. 2006, 142 (2): 797-806.PubMed CentralPubMedView ArticleGoogle Scholar
  47. Cizkova M, Pichova A, Vitova M, Hlavova M, Hendrychova J, Umysova D, Galova E, Sevcovicova A, Zachleder V, Umen JG, Bisova K: CDKA and CDKB kinases from Chlamydomonas reinhardtii are able to complement cdc28 temperature-sensitive mutants of Saccharomyces cerevisiae. Protoplasma. 2008, 232 (3–4): 183-191.PubMedView ArticleGoogle Scholar
  48. Bisova K, Krylov DM, Umen JG: Genome-wide annotation and expression profiling of cell cycle regulatory genes in Chlamydomonas reinhardtii. Plant Physiol. 2005, 137 (2): 475-491.PubMed CentralPubMedView ArticleGoogle Scholar
  49. Schaap P: Guanylyl cyclases across the tree of life. Front Biosci. 2005, 10: 1485-1498.PubMedView ArticleGoogle Scholar
  50. Shenroy AR, Visweswariah SS: Class III nucleotide cyclases in bacteria and archaebacteria: lineage-specific expansion of adenylyl cyclases and a dearth of guanylyl cyclases. FEBS Lett. 2004, 561 (1–3): 11-21.PubMedView ArticleGoogle Scholar
  51. Franklin KA, Whitelam GC: Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nature Genet. 2007, 39 (11): 1410-1413.PubMedView ArticleGoogle Scholar
  52. Nagatani A: Light-regulated nuclear localization of phytochromes. Curr Opin Plant Biol. 2004, 7 (6): 708-711.PubMedView ArticleGoogle Scholar
  53. Winands A, Wagner G: Phytochrome of the green alga Mougeotia: cDNA sequence, autoregulation and phylogenetic position. Plant Mol Biol. 1996, 32 (4): 589-597.PubMedView ArticleGoogle Scholar
  54. Kidd DG, Lagarias JC: Phytochrome from the green alga Mesotaenium caldariorum. J Biol Chem. 1990, 265 (12): 7029-7035.PubMedGoogle Scholar
  55. Casal JJ, Yanovsky MJ: Regulation of gene expression by light. Int J Dev Biol. 2005, 49 (5–6): 501-511.PubMedView ArticleGoogle Scholar
  56. Wu HP, Su YS, Chen HC, Chen YR, Wu CC, Lin WD, Tu SL: Genome-wide analysis of light-regulated alternative splicing mediated by photoreceptors in Physcomitrella patens. Genome Biol. 2014, 15 (1): R10-PubMed CentralPubMedView ArticleGoogle Scholar
  57. Jiao Y, Lau OS, Deng XW: Light-regulated transcriptional networks in higher plants. Nat Rev Genet. 2007, 8 (3): 217-230.PubMedView ArticleGoogle Scholar
  58. Lopez-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JA, Beemster GT, Bogre L, Shanahan H: Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell. 2008, 20 (4): 947-968.PubMed CentralPubMedView ArticleGoogle Scholar
  59. Ma L, Sun N, Liu X, Jiao Y, Zhao H, Deng XW: Organ-specific expression of Arabidopsis genome during development. Plant Physiol. 2005, 138 (1): 80-91.PubMed CentralPubMedView ArticleGoogle Scholar
  60. Kami C, Lorrain S, Hornitschek P, Fankhauser C: Light-regulated plant growth and development. Curr Top Dev Biol. 2010, 91: 29-66.PubMedView ArticleGoogle Scholar
  61. Molas ML, Kiss JZ, Correll MJ: Gene profiling of the red light signalling pathways in roots. J Exp Bot. 2006, 57 (12): 3217-3229.PubMedView ArticleGoogle Scholar
  62. Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH: Multiple transcription-factor genes are early targets of phytochrome A signaling. Proc Natl Acad Sci U S A. 2001, 98 (16): 9437-9442.PubMed CentralPubMedView ArticleGoogle Scholar
  63. Meyerowitz EM: Plants compared to animals: the broadest comparative study of development. Science. 2002, 295 (5559): 1482-1485.PubMedView ArticleGoogle Scholar
  64. Tam LW, Kirk DL: Identification of cell-type-specific genes of Volvox carteri and characterization of their expression during the asexual life cycle. Dev Biol. 1991, 145 (1): 51-66.PubMedView ArticleGoogle Scholar
  65. Meissner M, Stark K, Cresnar B, Kirk DL, Schmitt R: Volvox germline-specific genes that are putative targets of RegA repression encode chloroplast proteins. Curr Genet. 1999, 36 (6): 363-370.PubMedView ArticleGoogle Scholar
  66. Deng XW, Quail PH: Signalling in light-controlled development. Semin Cell Dev Biol. 1999, 10 (2): 121-129.PubMedView ArticleGoogle Scholar
  67. Neff MM, Fankhauser C, Chory J: Light: an indicator of time and place. Genes Dev. 2000, 14 (3): 257-271.PubMedGoogle Scholar
  68. Suetsugu N, Wada M: Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem. 2007, 388 (9): 927-935.PubMedView ArticleGoogle Scholar
  69. Franklin KA: Shade avoidance. New Phytologist. 2008, 179 (4): 930-944.PubMedView ArticleGoogle Scholar
  70. Hudson ME, Lisch DR, Quail PH: The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J. 2003, 34 (4): 453-471.PubMedView ArticleGoogle Scholar
  71. Quail PH: Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol. 2002, 3 (2): 85-93.PubMedView ArticleGoogle Scholar
  72. Duncan L, Nishii I, Howard A, Kirk D, Miller SM: Orthologs and paralogs of regA, a master cell-type regulatory gene in Volvox carteri. Curr Genet. 2006, 50 (1): 61-72.PubMedView ArticleGoogle Scholar
  73. Kirk MM, Stark K, Miller SM, Muller W, Taillon BE, Gruber H, Schmitt R, Kirk DL: regA, a Volvox gene that plays a central role in germ-soma differentiation, encodes a novel regulatory protein. Development. 1999, 126 (4): 639-647.PubMedGoogle Scholar
  74. Mittag M: Conserved circadian elements in phylogenetically diverse algae. Proc Natl Acad Sci U S A. 1996, 93 (25): 14401-14404.PubMed CentralPubMedView ArticleGoogle Scholar
  75. Zhao B, Schneid C, Iliev D, Schmidt EM, Wagner V, Wollnik F, Mittag M: The circadian RNA-binding protein CHLAMY 1 represents a novel type heteromer of RNA recognition motif and lysine homology domain-containing subunits. Eukaryot Cell. 2004, 3 (3): 815-825.PubMed CentralPubMedView ArticleGoogle Scholar
  76. Yakir E, Hassidim M, Melamed-Book N, Hilman D, Kron I, Green RM: Cell autonomous and cell-type specific circadian rhythms in Arabidopsis. Plant J. 2011, 68 (3): 520-531.PubMedView ArticleGoogle Scholar
  77. Sommer U, Gliwicz ZM: Long-range vertical migration of Volvox in tropical lake Cahora Bassa (Mozambique). Limnol Oceanogr. 1986, 31 (3): 650-653.View ArticleGoogle Scholar
  78. Moran MA, Miller WL: Resourceful heterotrophs make the most of light in the coastal ocean. Nat Rev Microbiol. 2007, 5 (10): 792-800.PubMedView ArticleGoogle Scholar
  79. Ragni M, D’Alcala MR: Light as an information carrier underwater. J Plankton Res. 2004, 26 (4): 433-443.View ArticleGoogle Scholar
  80. Suzuki T, Yamasaki K, Fujita S, Oda K, Iseki M, Yoshida K, Watanabe M, Daiyasu H, Toh H, Asamizu E, Tabata S, Miura K, Fukuzawa H, Nakamura S, Takahashi T: Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochem Biophys Res Commun. 2003, 301 (3): 711-717.PubMedView ArticleGoogle Scholar
  81. Luck M, Mathes T, Bruun S, Fudim R, Hagedorn R, Nguyen TM, Kateriya S, Kennis JT, Hildebrandt P, Hegemann P: A photochromic histidine kinase rhodopsin (HKR1) that is bimodally switched by UV and blue light. J Biol Chem. 2012, 287: 40083-40090.PubMed CentralPubMedView ArticleGoogle Scholar
  82. Roenneberg T, Foster RG: Twilight times: light and the circadian system. Photochem Photobiol. 1997, 66 (5): 549-561.PubMedView ArticleGoogle Scholar
  83. Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B: The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res. 2011, 109 (1–3): 133-149.PubMedView ArticleGoogle Scholar

Copyright

© Kianianmomeni; licensee BioMed Central Ltd. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Advertisement