Plant Physiol. (1982) 70, 1549-15530032-0889/82/70/1549/05/$00.50/0

Growth and Chromatic Adaptation of Nostoc sp. Strain MAC andthe Pigment Mutant R-MAC'

Received for publication March 1, 1982 and in revised form July 15, 1982

JUDITH A. KIPE-NOLT2, S. EDWARD STEVENS, JR.3, AND DONALD A. BRYANTMicrobiology Program, Department of Biochemistry, Microbiology, Molecular and Cell Biology,The Pennsylvania State University, University Park, Pennsylvania 16802

ABSTRACT

A spontaneous, stable, pigmentation mutant of Nostoc sp. strain MACwas isolated. Under various growth conditions, this mutant, R-MAC, hadsimilar phycoerythrin contents (relative to aliophycocyanin) but signifi-cantly lower phycocyanin contents (relative to allophycocyanin) than theparent strain. In saturating white light, the mutant grew more slowly thanthe parent strain. In nonsaturating red light, MAC grew with a shortergeneration time than the mutant; however, R-MAC grew more quickly innonsaturating green light.When the parental and mutant strains were grown in green light, the

phycoerythrin contents, relative to allophycocyanin, were significantlyhigher than the phycoerythrin contents of cells grown in red light. For bothstrains, the relative phycocyanin contents were only slightly higher for cellsgrown in red light than for cells grown in green light. These changescharacterize both MAC and R-MAC as belonging to chromatic adaptationgroup II: phycoerythrin synthesis alone photocontrolied.A comparative analysis of the phycobilisomes, isolated from cultures of

MAC and R-MAC grown in both red and green light, was performed bypolyacrylamide gel electrophoresis in the presence of 8.0 molar urea orsodium dodecyl sulfate. Consistent with the assignment of MAC and R-MAC to chromatic adaptation group II, no evidence for the synthesis ofred light-inducible phycocyanin subunits was found in either strain. Phy-cobilisomes isolated from MAC and R-MAC contained linker polypeptideswith relative molecular masses of 95, 34.5, 34, 32, and 29 kilodaltons.When grown in red light, phycobilisomes of the mutant R-MAC appearedto contain a slightly higher amount of the 32-kilodalton linker polypeptidethan did the phycobilisomes isolated from the parental strain under thesame conditions. The 3'..5-kilodalton linker polypeptide was totally absentfrom phycobilisomes isolated from cells of either MAC or R-MAC grownin green light.

In the cyanobacteria and the red and cryptophyte algae, phy-cobiliproteins function as photosynthetic accessory pigmentswhich transfer trapped light energy to protein-chlorophyll com-

plexes at the reaction centers. The phycobiliproteins can be di-vided into three major spectral classes on the basis of their longestwavelength absorption maxima. The PE4 exhibit adsorption max-

' This study was supported by Grants GM 23524 and GM 28609 fromthe National Institutes of Health and Grant 7900238 from the UnitedStates Department of Agriculture.

2 Present address: ICRISAT, Patancheru P. O., Andhra Pradesh, 502324, India.3To whom correspondence should be addressed.4Abbreviations: PE, phycoerythrin; APC, allophycocyanin; PC, phy-

cocyanin.

ima around 565 nm, the PC around 620 nm and the APC around650 nm. Further subdivisions of these three major classes arebased either upon the taxonomic origins of the organism whichserves as the source of the protein or upon the number andwavelength positions of the major visible absorption maxima (1 1).All cyanobacteria contain APC and C-phycocyanin, while all redalgae contain APC and C- or R-phycocyanin (11). Many cyano-bacteria and a few red algae do not synthesize phycoerythrin.

In the red algae and cyanobacteria, the phycobiliproteins ag-gregate to form supramolecular complexes referred to as phyco-bilisomes. Phycobilisomes are located on the stromal side of thephotosynthetic lamellae and are often observed in regular, parallelrows. The structure, composition, and function of phycobilisomeshave recently been reviewed by Gantt (8). Phycobilisomes fromseveral cyanobacteria (5, 12) and from the red alga Rhodellaviolacea (17) have been shown to consist of two types of substruc-tures: a core composed of three stacks of disc-shaped rings ar-ranged into a triangular array, and several rod-like stacks of disc-shaped molecules which radiate from each of two sides of thetriangular core in a hemidiscoidal arrangement. The core units arebelieved to be largely composed ofAPC, while the peripheral rodsare largely composed of PC (proximal to the core) and PE (at thedistal ends of the rods). Tandeau de Marsac and Cohen-Bazire(25) established the presence of a small number (4-8) of nonpig-mented polypeptides in cyanobacterial phycobilisomes, which intotal account for 10 to 15% (by weight) of the phycobilisomeprotein. These 'linker polypeptides' have been shown to play acritical role in phycobilisome assembly and structure (6, 15, 26,27, 29).Some cyanobacteria exhibit complementary chromatic adapta-

tion, a response in which the phycobiliprotein with an absorptionspectrum most nearly complementary to the energy spectrum ofthe available light is synthesized preferentially. Tandeau de Mar-sac (24) described three different types of responses to chromaticillumination. Some PE-containing cyanobacteria do not adaptchromatically (group I); the relative rates of PE, PC, and APCsynthesis are constant and characteristic for each strain. In orga-nisms from group II, only the synthesis of PE is modulated; therate of PE formation is higher in green light than in red light. Instrains from group III, light wavelength affects the rate of synthesisof both PC and PE; the rate of PE synthesis is higher in greenlight, while the rate of PC synthesis is higher in red light.

Pigment mutants of a number of different cyanobacteria havebeen isolated. They have proved to be useful in physiologicalstudies of photosynthetic pigments (18, 22) and in structuralstudies of the light-harvesting apparatus (26, 29). Growth andchromatic adaptation of Nostoc sp. strain MAC and the pigmentmutant R-MAC are compared in this study with the purpose offurther delineating our understanding of chromatic adaptationand phycobilisome structure.

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w

0 5z

w

540 580 620 660 700

WAVELENGTH (nm)FIG. 1. Whole cell absorbance spectra of MAC and R-MAC grown in

red light. Liquid cultures were grown in red light having a maximumintensity at 650 nm.

GREEN LIGHT

0-

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-)MAC

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FIG. 2. Whole cell absorbance spectra of MAC and R-MAC grown ingreen light. Liquid cultures were grown in green light having a maximumintensity at 550 nm.

MATERIALS AND METHODS

Organism. Nostoc sp. strain MAC, a generous gift of C. VanBaalen (University of Texas) was isolated by Bowyer and Skerman(2) from the coralloid roots of the cycad Macrozamia lucida. R-MAC is a spontaneous pigment mutant that was isolated from aplate incubated at low light intensity at room temperature.Media and Growth. Liquid cultures of MAC and R-MAC were

routinely grown in medium B of Stevens et al. (23) in a 35°Ccontrolled temperature water bath. Continuous agitation and CO2were provided by bubbling 4% C02-in-air (v/v) through thecultures. Illumination consisted of four F72T12 CW fluorescentlamps, giving a final light intensity of 4 x 10-2 ILE cm-2 s-'.Red (Rohm and Haas No. 2423) or green (Rohm and Haas No.

2092) Y8-inch-thick Plexiglas filters were put around the waterbaths for growth studies on chromatic adaptation. The green filterprovided maximum light intensity at 550 nm, while the red filterprovided maximum intensity at 650 nm. The final light intensityin both baths was matched to 0.5 x 102,uEcm2 s- by screening

the green light bath with window screening.Growth was measured turbidimetrically with a Bausch and

Lomb Spectronic 20 colorimeter at 720 nm or by determining dryweights.Pigment Determination. Whole cell absorbance spectra were

taken in 1-cm quartz cuvettes with scattering plates (21) of 3-mmwhite translucent Plexiglas (Rohm and Haas No. 7328) in a Cary

recording spectrophotometer model 14R. Estimates of the pigmentcontent of MAC and R-MAC were done as follows. Cell suspen-sions were concentrated by centrifugation at 1200g for 20 min andthe pellets were quick-frozen in liquid N2, thawed, and thensonicated for 3 min in a Bronson-12 ultrasonic bath. Followingcentrifugation at 12,000g for 30 min, absorbance spectra of thesupernatants were determined. Phycobiliprotein contents wereestimated using the simultaneous equations of Bennett and Bo-gorad (1). Chl was extracted with acetone as in Myers and Kratz(19). The absorption coefficient of MacKinney (16) was used todetermine Chl content.

Phycobilisome Isolation. The procedure for the isolation ofphycobilisomes was developed by Gantt et al. (9). All bufferscontained 1 mm EDTA, 3 mm NaN3, and 1 mm phenylmethylsul-fonyl fluoride. Cultures of MAC and R-MAC were grown in red,green, or white light. The cells were collected by centrifugationand washed two times with 0.5 M Na-K-phosphate buffer, pH 7.0.The cells were then resuspended to a concentration of about 0.1to 0.3 g (wet weight)/ml in 0.75 M Na-K-phosphate, pH 7.0.Following cell breakage with a French press (American Instru-ment) at 16,000 p.s.i., the extract was incubated in 1% Triton X-100 (v/v) for 10 min. Large fragments and cell debris wereremoved by centrifugation at 27,000g for 15 min. Supematant (5ml) from just under the floating Chl layer was then layered ontoa buffered sucrose step gradient. The gradient was prepared usingthe following sucrose concentrations made up in 0.75 M Na-K-phosphate: 2.0 M (5 ml), 1.0 M, (10 ml), 0.75 M (5 ml), 0.50 M, (5ml), and 0.25 M (5 ml). Gradients were centrifuged at 80,000g for16 h. Phycobilisomes formed a dark purple layer in the 1.0 Msucrose zone.

Polyacrylamide Gel Electrophoresis. Electrophoresis at pH 7.85on 5% polyacrylamide gels in the presence of 8.0 M urea wasperformed as described by Cohen-Bazire et al. (7). Samples wereprepared for electrophoresis as described (5), except that 5 mmdithioerythritol was included as a reducing agent instead of 10 mm2-mercaptoethanol. Gels were fixed and stained as described (4).

Polyacrylamide gel electrophoresis in the presence of SDS wasperformed on slab gels using the discontinuous buffer system ofLaemmli (14). The running gel (0.15 x 14 cniA contained a linearconcentration gradient (10-20%/o, w/v; acrylalnide:bisacrylamide,30:0.8) of acrylamide. Gels were stained as described by Yaman-aka et aL (28).

RESULTSLarge numbers of streak plates of Nostoc sp. strain MAC that

had been grown in low light intensities at room temperature wereexamined for the appearance of cells with unusual colorations. R-MAC was one of several spontaneous pigment mutants observed.When compared to the dark greenish brown color of the parentstrain, R-MAC had a more reddish tint. This mutant did notrevert to the parental type under any culture conditions. Althoughdistinctive color differences were observed, MAC and R-MAChad similar colony morphology, filament length, and cellularmorphology when observed with the light microscope.

In saturating white light (4 x 10-2 ILE cm-2 S-1), MAC had ageneration time of 7.4 h whereas R-MAC grew more slowly witha generation time of 8.6 h. In limiting red and green light (0.5 x10-2 ,uE cm-2 s-1), growth was much slower. In red light, MAChad a generation time of 16 h while R-MAC had a slower growthrate (generation time, 18.4 h). As can be seen from whole cellabsorbance spectra (Fig. 1), R-MAC had a lower A in the 620- to650-nm region than the parental strain. Cultures of MAC grownin red light had A peaks at 678, 625, and 575 nm and a shoulderat 550 nm. The same maxima were observed in spectra of R-MACgrown in red light with the addition of a shoulder at 648 nm.The generation time for R-MAC in green light was 16.5 h,

whereas the parent strain grew more slowly in this light environ-

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CHROMATIC ADAPTATION IN NOSTOC SP.

Table I. Pigment Content in MAC and R-MAC Grown in Red and Green LightPigment content was determined as described in "Materials and Methods." The results given are averages

from four experiments. Data extremes were + 1 for Chl; ±4 for phycobiliproteins.

Pigment Content

Chl PC APC PE PE/APC PC/APC PE/PCMACRed light 16 71 39 26 0.67 1.82 0.37Green light 16 47 34 59 1.74 1.38 1.26

R-MACRed light 17 44 56 39 0.70 0.79 0.89Green light 16 24 34 62 1.82 0.71 2.58

Pigment Ratios Assuming Constant APC Content

PC red light APC green light PE green light APC red lightAPC red light PC green light APC green light PE red light

MAC 1.31 2.60R-MAC 1.11 2.60

w

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a:

w B

w

450 500 550 600 650 700WAVELENGTH (nm)

FIG. 3. Absorbance spectra of intact phycobilisomes isolated fromMAC and R-MAC. Cultures were grown in white light. Phycobilisomeswere isolated as described in "Materials and Methods." A, Absorbancespectra of phycobilisomes from MAC in 0.75 M Na-K-phosphate buffer,pH 7.0, with 0.5 M sucrose; B, phycobilisomes from R-MAC in 0.75 M Na-K-phosphate buffer, pH 7.0, with 0.5 M sucrose.

ment with a generation time of 17.9 h. The whole cell absorbanceof R-MAC was higher than that of MAC in the green region ofthe spectrum (Fig. 2). Absorbance maxima for cultures of bothMAC and R-MAC grown in green light occurred at 678, 625, 575,and 550 nm. Although these absorption maxima were similar tothose observed for the red light-grown cultures, the spectra werevery different (Figs. 1 and 2). Red light-grown cultures had a

higher A at 620 nm than at 550 nm, while green light-growncultures had a higher A at 550 nm than at 620 nm.The phycobiliprotein and Chl contents of MAC and R-MAC

were determined after growth in red and green light (Table I).Cell dry weight/ml of culture was determined and pigment con-centrations were estimated as described in "Materials andMethods." The Chl content was constant (16-17 mg/g) in bothMAC and R-MAC when cells were grown in either red or green

light. In red light-grown MAC and R-MAC, the concentration ofPE was lower than the concentration of PC. This difference was

more pronounced in MAC, which had a PE/PC ratio of 0.37, thanin R-MAC where the PE/PC ratio was 0.89. The PC concentrationin R-MAC was somewhat lower than in MAC, the APC contentwas significantly higher, and the PE concentration was a littlehigher. In green light-grown cultures of R-MAC and MAC, theconcentrations of PE were higher than the concentration of PC; inthis light environment, the difference was again more pronouncedin R-MAC. The ratio of PE/PC was 2.58 in R-MAC as comparedto 1.26 in MAC. The APC contents were the same in green light-grown cells of both strains.

Phycobilisomes were isolated from white light-grown culturesof MAC and R-MAC. Phycobilisomes isolated from the parentaland mutant strain under these conditions were approximatelyequal in size as indicated by their similar migrations throughsucrose gradients. Their appearance in the electron microscope,after fixation with glutaraldehyde and negative staining withuranyl acetate, was also similar (not shown). The absorbancespectrum of phycobilisomes isolated from white light-grown cellsofMAC is shown in Figure 3A. As observed in whole cell spectra,a double-peaked (550 and 570 nm) PE A was noted. A peak at620 nm and a shoulder at 645 nm demonstrated the presence ofPC and APC. No Chl was present. Phycobilisomes isolated fromwhite light-grown cells ofR-MAC also exhibited a double-peakedPE A (550 and 570 nm); secondary absorption maxima were notedat 610 and 650 nm (Fig. 3B).The ratios of PE/PC were determined for whole cell extracts

and isolated phycobilisomes from MAC and R-MAC. A PE/PCratio of 1.3 was observed in both cell extracts and isolated phy-cobilisomes from MAC grown in white light. This ratio was muchlower than that observed in both cell extracts and for phycobili-somes isolated from R-MAC. In R-MAC cells grown in whitelight, the PE/PC ratio was significantly higher (2.4-2.7).

Phycobilisomes, isolated from cells ofMAC and R-MAC grownin red, green, or white light, were analyzed by polyacrylamide gelelectrophoresis in the presence of 8.0 M urea at pH 7.85 or in thepresence of SDS. Phycobilisomes isolated from cells of MACgrown in red light were resolved by electrophoresis in the presenceof 8.0 M urea into four blue bands (the a and ,B subunits of PCand APC, respectively) and two red bands (the a and ,8 subunitsof PE) as shown in Figure 4A. After the gels were stained withCoomassie Blue, additional polypeptides were observed whichmay correspond to the linker polypeptides of the Nostoc sp.phycobilisomes (see below and Fig. 4B). The pattern obtainedwith phycobilisomes isolated from R-MAC was essentially iden-

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__

1 2 3 4 5Mr* 10

9485

34.5343229

PEPCPEPC

APC E4.

A BFIG. 4. Analysis of MAC and R-MAC phycobilisomes by polyacrylamide gel electrophoresis. A, Polyacrylamide gel electrophoresis of isolated

phycobilisomes at pH 7.85 in the presence of 8.0 M urea. Phycobilisomes were isolated from MAC cells grown in red light (gel 1) or green light (gel 2)and from R-MAC cells grown in red light (gel 3) or green light (gel 4). Phycobiliprotein subunit assignments are shown at the left. B, Polyacrylamidegel electrophoresis of isolated phycobilisomes in the presence of SDS. Phycobilisomes were isolated from MAC cells grown in red light (lane 1) or greenlight (lane 4) and from R-MAC cells grown in red light (lane 2) or green light (lane 5). Mol wt markers (lane 3) are phosphorylase b (92 kD), BSA (68kD), ovalbumin (43 kD), carbonic anhydrase (30 kD), soybean trypsin inhibitor (21.5 kD), and lysozyme (14.3 kD). Relative molecular masses of linkerpolypeptides and phycobiliprotein subunit assignments are shown at the left.

tical except that the PE subunit bands were somewhat moreintense. When phycobilisomes, isolated from MAC or R-MACcultures grown in green light, were analyzed by polyacrylamidegel electrophoresis in the presence of 8.0 M urea, the bandingpatterns of the colored phycobiliprotein subunits were similar tothose obtained for the phycobilisomes from red light-grown cells.The red PE subunit bands were more intense, however, and thea and f8 subunits of PC were somewhat less intense than forphycobilisomes from red light-grown cells.The results of an analysis ofMAC and R-MAC phycobilisomes

by polyacrylamide gel electrophoresis in the presence of SDS areshown in Figure 4B. Nostoc sp. strain MAC phycobilisomes havebeen reported to contain uncolored or linker polypeptides withmolecular masses of 94, 34.5, 34, 32, and 29 kD (13). Our resultsare in agreement with these reported values. Additional polypep-tides, observed in variable amounts, with molecular masses ofabout 85, 28.5, and 26.5 kD are apparently proteolytic degradationproducts of the 94-kD and 29-kD polypeptides. Glick and Zilin-skas (13) have reported that these polypeptides are particularlysensitive to proteolysis in Nostoc sp. strain MAC.

Phycobilisomes isolated from cultures of the parental and mu-tant strains grown in red light were very similar. Although thephycobilisomes of red light-grown R-MAC and MAC containeda similar proportion of PE, the R-MAC phycobilisomes containedsignificantly more of the 32-kD linker polypeptide. The phyco-bilisomes isolated from green light-grown cultures of MAC andR-MAC were identical when analyzed by polyacrylamide gelelectrophoresis in the presence of SDS. A striking result obtainedfor both strains was the total absence of the 34.5-kD polypeptide

from these phycobilisomes. The absence of this polypeptide doesnot appear to have been the result of proteolysis, since thesephycobilisome samples were given identical treatments and pro-cessed in parallel with samples derived from red light-grown cellsin which the 34.5-kD polypeptide was easily demonstrable.

DISCUSSION

R-MAC did not grow as well as the parent strain under lightsaturating conditions. However, R-MAC did grow with a shortergeneration time than MAC in green light. This may have beenbecause of the increased PE concentration in R-MAC or a com-bination of the increased PE and decreased PC concentrations.This selective advantage of R-MAC in low intensity green lightmay explain its spontaneous appearance and growth on plates influorescent room light, since the fluorescent lamps used have ahigh emission in the green-blue region of the spectrum.The data in Table I suggest that Nostoc sp. strain MAC is

capable of making some adjustments in PC and PE contents inorder to use the available light optimally. Since the APC-contain-ing core structures ofcyanobacterial phycobilisomes do not appearto change significantly during chromatic adaptation (5), APC is aconvenient reference for measuring the magnitude of changes inPC and PE contents. Adjusted for the difference in APC contents,the ratio (1.31) of PC contents for MAC cells grown in red andgreen light falls within the range (1-1.3) of values observed forstrains assigned to chromatic adaptation group II by Tandeau deMarsac (24). Although MAC synthesizes PE preferentially ingreen light, the content of PE in red light-grown cells is relatively

APCPC

I..... Af m W.

PE } $

PEPC

APC

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CHROMATIC ADAPTATION IN NOSTOC SP.

high: approximately 40% of the value observed for cells grown ingreen light.

For the spontaneous mutant R-MAC, the PE content of cellsgrown in green light is essentially identical with that of theparental strain. Moreover, red light-grown cells of R-MAC havea PE content, relative to APC, which is very similar to thatobserved for the parent strain. Whether grown in red or greenlight, R-MAC has a reduced concentration of PC (relative toAPC) relative to the parental strain. As observed for the parentalstrain, R-MAC synthesizes slightly more PC, relative to APC,when grown in red light. Thus, the spontaneous mutant R-MACappears more reddish brown in color, not from the overproductionof PE, but from its reduced level of synthesis of PC.When grown in red light, the mutant R-MAC produces all

phycobiliproteins in greater amounts relative to Chl. The PC/APC ratio, however, is essentially the same as that observed forcells grown in green light. Thus, when R-MAC is grown in redlight, the organism apparently compensates for its reduced capac-ity to synthesize PC by making more phycobilisomes per unit Chl.These observations indicate the importance of both complemen-tary chromatic adaptation and intensity adaptation mechanismsin optimizing the light-harvesting antennae of Nostoc sp. strainMAC.From their work with mutants ofAphanothece stagnia, Rohatgi

and Singh (20) proposed that the genetic controls in the synthesisof PC and PE are unlinked. In the mutants which they isolated,the synthesis of only one of the two pigments was affected. Glazerand co-workers (10, 26) have described a series of mutants ofSynechocystis 6701 which have PE contents between 0%o and 53%of the wild-type level. The PC/APC ratios for these mutantsindicate that PC synthesis is unaffected by the changes in the levelof expression of the PE genes. The results described above for themutant R-MAC are in agreement with these studies, inasmuch asthe level of expression of PC but not PE seems to have beenaffected in the spontaneous mutant.The results of an analysis of phycobilisomes of Nostoc sp. strain

MAC and the spontaneous mutant R-MAC by polyacrylamidegel electrophoresis in the presence of 8.0 M urea or SDS areconsistent with the assignment of Nostoc sp. strain MAC tochromatic adaptation group II: PE synthesis alone photocontrolled(see Refs. 3 and 24). In the presence of either denaturant, onlyfour blue-colored phycobiliprotein subunits, which correspondedto the a and I8 subunits of both APC and PC, were resolved. Allblue-colored bands observed on gels for samples derived from redlight-grown cells were also observed on gels for samples derivedfrom green light-grown cells. Hence, there is no evidence to suggestthat Nostoc sp. strain MAC synthesizes a phycocyanin specieswhich is specifically induced during growth in red light as hasbeen observed for most strains of chromatic adaptation groupIII:PE and PC synthesis photocontrolled (see Refs. 3 and 24).When examined by polyacrylamide gel electrophoresis in the

presence of SDS, the phycobilisomes of MAC and R-MAC werevery similar. The only significant difference was the elevatedcontent of the 32-kD linker polypeptide in R-MAC phycobili-somes isolated from cells grown in red light. Phycobilisomes,isolated from green light-grown cultures of either the parental ormutant strain, do not contain the 34.5-kD linker polypeptide butdo contain increased amounts of the 34- and 32-kD linker poly-peptides. This observation is in agreement with the findings ofZilinskas and co-workers (13, 30). Their studies suggest that the34.5-kD linker polypeptide is involved in PC-PC binding whilethe 34- and 32-kD linker polypeptides are more involved in PE-

PE and PE-PC interactions in the peripheral rod assemblies of theNostoc sp. strain MAC phycobilisome.

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