Cereal phytochromes: targets ofselection, targets for manipulation?Ruairidh J.H. Sawers, Moira J. Sheehan and Thomas P. Brutnell

Boyce Thompson Institute, Cornell University, Tower Road, Ithaca, NY 14853, USA

Plants respond to shading through an adaptive syn-

drome termed shade avoidance. In high-density crop

plantings, shade avoidance generally increases exten-

sion growth at the expense of yield and can be at odds

with the agronomic performance of the crop as a whole.

Studies in Arabidopsis are beginning to reveal the

essential role phytochromes play in regulating this

process and to identify genes underlying the response.

In this article, we focus on how phytochrome signaling

networks have been targeted in cereal breeding pro-

grams in the past and discuss the potential to alter these

pathways through breeding and transgenic manipu-

lation to develop crops that perform better under typical

high density conditions.

New tools for crop improvement

Plants must constantly monitor and adapt to changes intheir light environment [1,2]. In recent years, studies inArabidopsis have identified a complex network of blue,red, far-red and ultraviolet (UV) sensing photoreceptorsthat transduce light signals into changes in gene tran-scription, protein stability and hormone action [3,4].Although our understanding of light signal transductionpathways in major crop plants is less complete than inArabidopsis, advances in genomics afford new opportuni-ties for investigating these networks. A complete genomesequence is now available for rice (Oryza sativa) [5,6] andrapid progress is being made deciphering the gene-richregions of maize (Zea mays) [7]. In addition, extensiveexpressed sequence tag (EST) collections have beenassembled for several grasses, including rice, maize,barley (Hordeum vulgare), rye (Secale cereale), sorghum(Sorghum bicolor) and wheat (Triticum aestivum) (http://www.tigr.org/tdb/tgi/plant.shtml). Large transposon andT-DNA insertion libraries [8,9], EMS (ethyl methanesulfonate) populations for TILLING (targeting inducedlocal lesions in genomes) [10] and improvements in croptransformation technologies provide additional opportuni-ties to examine and manipulate gene function. Further-more, gene expression profiling platforms such asmicroarrays and serial analysis of gene expression(SAGE) analysis, together with advances in proteomicsand metabolomics, will provide detailed blueprints forengineering improved crop germ plasm in the yearsahead. These studies are beginning to reveal how artificialselection, genetic drift and polyploidization events have

Corresponding author: Brutnell, T.P. (tpb8@cornell.edu).

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reshaped crop light signal transduction networks in thepast. What remains to be seen is how the manipulation ofthese signaling pathways can be further exploited toimprove crop performance.

Phytochrome signal transduction pathways

Plant phytochromes are conjugates of a PHY apoproteincovalently attached to the linear tetrapyrrole chromo-phore 3E-phytochromobilin (PFB) [11]. They accumulatecytosolically as dimers in an inactive state. Incident red orfar-red light results in a reversible isomerization of thePFB chromophore and subsequent changes to proteinactivity and subcellular localization. The biochemical andmolecular bases of phytochrome signaling have beenextensively reviewed in recent publications [12–14].

In Arabidopsis, the phytochrome family consists of fivegenes (PHYA, PHYB, PHYC, PHYD and PHYE) [15,16].Comparative phylogenetic analyses have allowed furthergrouping of the PHY genes into four subfamilies (PHYA;PHYB and PHYD; PHYC and PHYF; and PHYE) [17,18].The PHY gene family is rapidly evolving and shows variedstructure in different plant taxa (Figure 1). In severaleudicot lineages, some PHY subfamilies appear to havebeen lost [17,19–22]. In the grasses, three of the foursubfamilies are present: PhyA, PhyB and PhyC [23–26]. Inmaize, an ancient genome duplication [27] has increasedthe family size to six (PhyA1, PhyA2, PhyB1, PhyB2,PhyC1 and PhyC2) [28]. Variations in gene familycomposition and size have contributed to divergence ofPHY gene function, which suggest that functional assign-ments to individual family members cannot be extra-polated across taxa.

Although the mechanism of photoconversion is believedto be common to all phytochromes, genetic analyses(predominantly in Arabidopsis) have shown that differentfamily members have distinct, overlapping and evenantagonistic roles during plant development [29]. Theemerging picture is one of a complex network of photo-receptor cross talk and interaction mediating manyresponses [30]. In maize, the presence of duplicated PHYgene family homeologs (orthologs from two speciesbrought together in one genome during a hybridizationevent such as allopolyploidization) has probably facili-tated the divergence and specialization of gene function[28] (Figure 1). For instance, overlapping expressionpatterns of PHY homeologs might allow a specializationof function without a concomitant loss in existing activity[31]. However, the isolation and characterization of PHY

Review TRENDS in Plant Science Vol.10 No.3 March 2005

. doi:10.1016/j.tplants.2005.01.004

Homologs

Co-orthologs

ParalogsHomeologs

A C E D B A C B A1A2 C1 C2 B1 B2

Arabidopsis Rice and sorghum Maize

TRENDS in Plant Science

Figure 1. Phytochrome gene family structure. All the genes represented are

homologs in that they all share a common PHY ancestor. Genes highlighted in red

in Arabidopsis are paralogs. They aremore closely related to each other than to any

other PHY genes. In maize, there are two copies of each PHY gene and each gene

pair could be considered to be paralogous. However, the maize genome is likely to

be a product of an ancient tetraploidization event [27] following hybridization of two

related grass species, each carrying a single set of PhyA, PhyB and PhyC genes.

These gene pairs now reside on syntenic regions of themaize genome derived from

the homologous chromosomes of each parental genome and thus are defined as

homeologs (blue) [28]. An example of co-orthology is illustrated for the PhyB genes

(green). The single-copy sorghum and rice PHYB genes are equally related to the

two Arabidopsis genes PHYD and PHYB. Similarly, the maize PhyB1 and PhyB2

genes are equally related to Arabidopsis PHYD and PHYB. Terminology used to

describe homology: co-orthologs, paralogs produced by duplications of orthologs

subsequent to a given speciation event; homeologs, orthologs from two species

brought together in one genome during a hybridization event such as allopoly-

ploidization; homologs, two or more genes that are descendants of an ancestral

gene; orthologs, genes from two different species that derive from a single gene in

the last common ancestor; paralogs, genes that are derived from a single gene that

was duplicated within a genome.

Review TRENDS in Plant Science Vol.10 No.3 March 2005 139

familymutants in thegrasseshasonly justbegun[26,32,33].These studies are essential if we are to discover the role ofPHY genes in the regulation of developmental processesthat are unique to a given species or group of plants,particularly those directly related to the agronomicperformance of these crops (e.g. light-mediated develop-ment of brace roots in rice [32]).

Phytochrome control of flowering time in cereals

Thedomestication of crop grasses has resulted in changes totheir distribution and ecology. Historically, the mostsignificant effect of human selectionupon cropphotosensorysystems has been the generation of lines exhibiting novelvariations in flowering time [34–37]. Cereal crops can bedivided into temperate species (e.g. wheat, barley and rye)that flower preferentially under long day (LD) conditionsand those of semitropical origin (e.g. maize, rice andsorghum) that flower in response to short days (SD) [34,36].Such flowering strategies synchronize reproductionwithin a population and allow adaptation to seasonalfluctuations in resources and environmental stress. Theselection of day-length-insensitive varieties, in whichflowering is not governed by photoperiod, has allowedthe spread of cereal crops beyond their areas of origin(e.g. maize and sorghum to the northern USA, wheat tosouthern Europe) and the adoption of novel reproductivestrategies (e.g. spring barley and winter wheat) [34,35].

Genetic analyses of Arabidopsis have defined threedistinct but integrated pathways that regulate control of

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flowering time: the day-length pathway, the vernalizationpathway and the endogenous pathway [37]. Initialcomparative studies suggested that many of the com-ponents defined in Arabidopsis are universally present inflowering plants [38–40]. However, sequence analysis ofthe rice genome has yielded the surprising finding thatseveral Arabidopsis floral regulators have no clearorthologs in rice (including FLC, AGL20, CAL, UFO andSUP) [5] or have taken on new roles in the regulation offlowering time (e.g. CO) [41].

In several crop grasses, selection for day-length-insensitive flowering has identified mutants in phyto-chrome photoreceptors [26,33,42]. Day-length insensitivityrelieves the normal repression of flowering under non-permissive conditions (whether SD or LD). Typically, day-length-insensitive lines show little difference in floweringcompared with sensitive lines under permissive daylength [42,43]. The Ma3 gene of sorghum, originallyidentified as one of six loci controlling flowering time,has been shown to encode PHYB [26]. Plants homozygousfor the recessive allele ma3

R are nearly completelyphotoperiod insensitive and flower early under LDconditions. Similarly, the early-flowering barley genotypeBMDR-1 shows photoperiod insensitivity associated witha light-labile phyB protein (although, in this instance, thegreatest acceleration of flowering is seen under SDconditions) [33]. It is interesting that mapping studieshave suggested that BMDR-1 and eak (Ppd-H2) are allelic,which was originally isolated on the basis of variationbetween winter and spring barley varieties [34]. In riceand maize, mutants have been defined that reduce thetotal active phytochrome pool because of blocks in thesynthesis of the PFB chromophore [42–44]. Characteriz-ation of the chromophore-deficient early-flowering se5mutant of rice offers further evidence that phytochromesnormally delay flowering [42,45]. The maize chromophore-deficient elm1 mutant also flowers early under non-permissive day lengths [43]. Although maize is oftenconsidered day neutral, the elm1 allele still acceleratesflowering when converged into standard US inbreds thatare considered photoperiod insensitive. Thus, it appearsthat a loss in phytochrome activity can accelerate flower-ing time in many crop plants. Indeed, a recent survey ofsemitropical, tropical and North American maize inbredsrevealed that lines adapted to more northern temperateenvironments displayed reduced photomorphogenicresponses relative to semitropical varieties [46].

Phytochrome control of the shade avoidance response

in cereals

Plants growing close to one another exhibit severaladaptive responses to maximize their ability to competefor limited resources [47,48]. Shaded plants are typicallymore elongated and show reduced branching, increasedinternode elongation and an acceleration of flowering.Collectively, these responses have been termed the shadeavoidance syndrome. Shade avoidance is initiated inresponse to a decreased ratio of red:far-red incident lightthat results from the absorbance of red light by chloro-phyll in the surrounding vegetation. Although initiallyconsidered to be a phyB-mediated response, multiple

Review TRENDS in Plant Science Vol.10 No.3 March 2005140

phytochromes are now believed to play a role [49].Evidence is also emerging that several hormonal path-ways are integrated in the control of this aspect ofdevelopmental plasticity, including auxin, gibberellinsand ethylene [50–52].

Recently, gene expression profiling has been used toidentify components of the shade avoidance pathway inArabidopsis [53,54]. These studies have identified bothearly and late acting genes that regulate responses tovegetative shade. Detailed characterizations of two Ara-bidopsis transcription factors (ATHB-2 and PIL1) suggestthat shade avoidance responses are initiated by transcrip-tional changes following a decrease in the ratio of red tofar-red light [54,55]. In addition, genetic screens inArabidopsis have identified the gene PHYTOCHROMEAND FLOWERING TIME1 (PFT1) as a component of theshade avoidance pathway that acts downstream of PhyBto regulate flowering time in response to changes in lightquality [56]. PhyA and PhyBmight play antagonistic rolesin the regulation of shade-responsive genes [53],suggesting a complex interplay between photoreceptorsand downstream effectors. Targeted disruption of thegrass orthologs of Arabidopsis genes mediating shadeavoidance responses is likely to provide clues to theconservation and divergence of shade avoidance responsepathways across these distantly related groups.

Shade avoidance responses might be detrimental tocrop yield under high-density plantings because a repar-titioning of resources to stem growth would probablydecrease yield [47,57]. As a result, shade avoidance hasbecome a target for transgenic manipulation [58–61].Although traditional breeding programs have selectedfor increased performance under high planting density[62,63], yield increases appear to be due to increasedtolerance for limited resources and not an ablation ofshade avoidance responses. For example, temperatemaizevarieties retain the ability to monitor far-red light andalter leaf angle, perhaps through an auxin-mediatedpathway, to maximize light interception in high densitystands [64,65].

Strategies to identify genes controlling light-regulated

development in cereals

In spite of the identification of several light-signalingmutants in Arabidopsis, there is still only limitedinformation about the variation of photoreceptor signalingfound in natural populations. To explore this potentialdiversity, researchers are beginning to survey populationsto link genetic variation to phenotypic variation [66,67].Surveys of genetically diverse populations can be used toidentify novel allelic variants that might have adaptivevalue [66]. Techniques such as quantitative trait locus(QTL) analysis [68] and association analysis [69] are nowbeing applied to the investigation of light signal transduc-tion networks.

QTL analysis uses molecular markers to identifylinkage between genetic and phenotypic variation in amapping population [70,71]. In studies using recombinantinbred (RI) populations, the resolution of QTLs depends onthe markers available and on the extent of recombinationobtained within the population. The identification of QTLs

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also depends on the extent and nature of allelic variationpresent in the population. For instance, the blue lightphotoreceptor CRY2 was identified as a QTL controllingflowering time in a mapping population containing a rarelight-stable allele [68]. In surveys of the light response inArabidopsis, many QTLs have been identified that controlhypocotyl elongation in response to red, far-red, blue andwhite light, but few map to the same chromosomal region[72]. Thus, each RI population has the potential to revealnovel variation contributing to phenotypic variation. Inseveral grass species, QTL analyses have been useful inthe identification of regions contributing to flowering timevariation [35,39,73,74]. As large-scale genome sequencingefforts progress and high-resolution mapping populationsbecome available, it is becoming increasingly feasible toidentify the genes underlying QTLs in crop species [75,76].

Many QTL studies are limited by the variation presentbetween the two parents of the mapping population used.By contrast, the techniques of association analysis havebeen developed to exploit fully the rich allelic diversityfound in natural populations [77]. DNA polymorphismsare used to identify haplotypes of a candidate genebelieved to underlie a trait of interest within a diversepopulation. Statistical methods are then used to derive acorrelation between haplotype and phenotype [77]. Associ-ation approaches have been successfully used to dissectflowering time variation in maize [78] and have greatpotential to identify allelic variation present in naturalpopulations.

Strategies for improving agronomic performance by

manipulation of light signaling pathways

The potential for future modification of light signalingpathways depends on the remaining developmentalplasticity within a given species. For instance, thechromophore-deficient se5 mutant has severely reducedphytochrome pools, whereas the ma3

R mutant of sorghumis deficient only in phyB activity. In both instances, alesion in phytochrome signaling results in early flowering.However, in the case of ma3

R, functional phyA and phyCproteins are still present and might serve as targets forfurther manipulation or selection, whereas, in se5,modification of phytochrome apoprotein genes would beexpected to have little or no additional effect. Althoughthis is an extreme and oversimplified scenario, the effectsof manipulating light signaling pathways in a givenspecies or cultivar will always depend on the targets ofprevious selection.

Traditional breeding and QTL studies have implicatedseveral loci in the light modulation of crop development.However, it should be realized that such approaches arelimited by available diversity and by genetic redundancy.The advent of transgenic approaches offers the ability tomanipulate targets that might have been previouslymasked by genetic redundancy or lack of diversity [59].For example, RNA interference or antisense-mediatedrepression of entire gene families and the introduction ofgain-of-function alleles of redundant genes have thepotential to reshape breeding programs in many cropspecies with large and highly redundant genomes. More-subtle manipulations could also be achieved by driving

Review TRENDS in Plant Science Vol.10 No.3 March 2005 141

transgene expression with tissue-specific promoters orwith promoters that are active early or late in vegetativedevelopment. Thus, it might be possible to maintain shadeavoidance responses during seedling establishment but toattenuate the responses as the canopy becomes moredense and the red to far-red ratio begins to decrease.

Comparative genetics has identified many phyto-chrome family members that are conserved betweenspecies (Figure 1). However, even if genes and theirmodes of action are conserved, the relationship between adevelopmental response and its effect on any givenagronomic trait depends on the species under consider-ation. For example, PHYA overexpression can causedwarfing and increased ‘bushiness’ in both tomato [79]and tobacco [58,80]. In one tomato study, such changes inplant architecture occur at the expense of fruit size andtherefore yield. However, in tobacco, a greater allocation ofresources to leaf growth results in an increase in theproportion of useful biomass. When comparing the modelspecies Arabidopsis to the cereals, there are severalimmediately evident differences in growth habit andarchitecture that make it impossible to generalize poten-tial benefits in manipulating phytochrome signalingpathways (Figure 2). Even within the grasses, it is difficultto generalize because domestication has reshaped manyaspects of plant development and physiology. This point isillustrated by comparing the architecture of maize andrice. In rice, increased tillering (branching) is associatedwith increased panicle production and therefore potentialyield gains. In maize, increased tillering results in super-fluous vegetative growth at the expense of reproductivedevelopment. Thus, an alteration in phytochrome signal-

Figure 2. Plant architecture and fruit morphology. (a) Maize (Zea mays) exhibits a predo

inflorescence (tassel) and one ormore female lateral inflorescences (ears). (b) Rice (Oryza

(tillered) and the flowers are borne on a single terminal inflorescence (panicle). (c) Ara

Multiple axillary meristems produce several lateral inflorescences that give rise to terti

Arabidopsis silique are shown.

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ing pathways that leads to decreased tillering might leadto increased yield in maize but to decreased yield in rice.

It remains to be determined whether attempts toengineer light-dependent traits are best served bymanipulating the photoreceptors or the targets of theiraction. The pleiotropic consequences of phytochromemanipulation can make it difficult to separate desirabletraits from linked detrimental effects. For example, aphyB mutant of sorghum and a chromophore-deficientmutant of maize flower early, but also display morefrequent lodging owing to increased internode elongation[26,43]. Nevertheless, sensory systems such as thephytochromes lie at the interface between endogenousdevelopmental pathways and the environmental cues thatmodulate them. Thus, manipulating phytochromes mightbe considered to be analogous to manipulating the lightenvironment itself. Such manipulations will not inthemselves alter the developmental potential of cropspecies but will modulate existing or latent patterns ofdevelopment (e.g. flowering of short day plants under LDconditions or limited elongation under shady conditions).Conceptually, manipulation at the sensory level canharness the potential of systems-level controls to targeta particular trait while maintaining plasticity of down-stream pathways. In practical terms, entire develop-mental syndromes can be induced without the need for acomplete understanding of the underlying components orthe need for multiple genetic manipulations. Ultimately,the agronomic success of attempts to manipulate light-signaling pathways will depend not only on a solidtheoretical basis but also on empirical tests of geneticmanipulations in a field setting.

minantly unbranched morphology, with a single main axis bearing a terminal male

sativa), by contrast, displays a typical grass architecture. Plants are highly branched

bidopsis grows in a rosette during vegetative growth and bolts before flowering.

ary inflorescences and flowers. Expanded views of the maize ear, rice panicle and

Review TRENDS in Plant Science Vol.10 No.3 March 2005142

Conclusions and prospects for future directions

Molecular genetic studies of Arabidopsis over the pastdecade have identified many ubiquitous components ofplant light signaling systems. Recent advances in themolecular characterization of crop species, notably riceand maize, are beginning to elucidate the commonalitiesbetween these plants and Arabidopsis, and, perhaps mostsignificantly, the areas of divergence between them.Furthermore, genetic techniques such as QTL analysisand association analysis are likely to lead to theidentification of loci that contribute directly to agronomicperformance without the need to formulate a prioriassumptions, and to the identification of novel or rarealleles that provide insight into phytochrome gene func-tion. A fundamental understanding of light responsepathways and knowledge of the underlying geneticvariation present in domesticated species will help toguide breeding programs towards the creation of varietiesthat are more fully integrated with the demands ofmodern cultivation.

Acknowledgements

We thank SusanMcCouch and Jeff Doyle for helpful discussions, and JakeMace for comments on the manuscript. Our work on phytochromesignaling pathways has been supported by the National ScienceFoundation (IBN-0110297).

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