468 The Plant Cell

LETTER TO THE EDITOR

Spotlight on Phytochrome Nomenclature

For many years after its discovery over phogenic mutants and transgenic plants teria1 system of gene nomenclature four decades ago, the regulatory pho- overexpressing different phytochromes (Sharrock and Quail, 1989; Quail, 1991, toreceptor phytochrome was widely have established that individual family 1994). However, as increasing numbers considered, implicitly or otherwise, to be members perform discrete photosensory of publications on the different a single molecular species (Sage, 1992). functions in interpreting and processing phytochrome family members have ap- However, steadily accumulating evidence information from the light environment peared from multiple laboratories, a from physiological, spectrophotometric, (Somers et al., 1991; McCormac et al., variety of nomenclature systems and sym- biochemical, and immunochemical studies 1992, 1993; Smith, 1992; Dehesh et al., bols have been used to describe not only made it increasingly difficult to reconcile 1993; Nagatani et al., 1993; Parks and the genes themselves, but also the gene the diversity of phytochrome-mediated Quail, 1993; Reed et al., 1993, 1994; products and photochemical forms of the responses with the action of asingle pho- Whitelam et al., 1993). individual family members. We believe toreceptor species (Smith and Whitelam, In Arabidopsis, the phytochrome poly- that it is timely, therefore, to implement 1990; Quail, 1991). There is now direct mo- peptide is encoded by a family of five a more standardized terminology to de- lecular evidence that the phytochrome genes (Sharrock and Quail, 1989; Clack scribe the phytochrome system. In polypeptide is encoded by multiple, diver- et al., 1994). These genes were initially addition, the recent demonstration that a gent genes, at least in higher plants (Quail, designated phyA, phyB, phyC, phyD, and series of photomorphogenic mutants of 1994). Moreover, studies with photomor- phyf (note lower case), based on the bac- Arabidopsis, isolated independently in

Table 1. Proposed Phytochrome Nomenclaturea Molecular Entity Designation Description Wild-type genes PHY Generic symbol for unknown, undesignated, or, collectively, all wild-type phytochrome genes. PHYA, PHYB, etc. Subfamily A, Subfamily B, etc. PHYA1, etc. Member number 1 of subfamily A, in cases where there are multiple closely related wild-type sequences of this subfamily at multiple loci in a single genome (e.g., oats, in which there are at least four PHYA sequences that are 98% identical), etc. Mutant genes PhY Generic or collective symbol for mutant phytochrome genes. (alleles) phyA-1, etc. Mutant allele number 1 at the A locus, etc. phyB1-1, etc. Mutant allele number 1 at the B1 locus, etc. Transcripts PHY mRNA Generic or collective symbol for mature phytochrome transcripts encoded by PHY genes. PHYA mRNA, etc. Mature transcript encoded by the PHYA gene, etc. Apoprotein PHY, PHY apoprotein, or Generic or collective symbols for phytochrome polypeptide encoded by PHY genes. apophytochrome PHYA, PHYA apoprotein, or Polypeptide encoded by the PHYA gene, etc. apophytochrome A, etc. Holoprotein phytochrome or phy Generic or collective symbols for fully assembled, photoreversible chromoprotein (holoprotein) with chromophore covalently attached to PHY apoprotein. phytochrome A or phyA, etc. Fully assembled chromoprotein (holoprotein) with chromophore covalently attached to PHYA apoprotein, etc. Photochemical Pr Generic or collective symbol for the red light-absorbing form of the phytochromes. forms Pf r Generic or collective symbol for the far-red-light-absorbing form of the phytochromes. PrA, etc. Red light-absorbing form of phytochrome A, etc. PfrA, etc. Far-red-light-absorbing form of phytochrome A, etc. PrB, etc. Red light-absorbing form of phytochrome B, etc. a Based on the Arabidopsis gene nomenclature system (which is derived in turn from the yeast system). Table modified from Quail (1994). April 1994 469

LETTER TO THE EDITOR

several laboratories and given various Table 2. New Designations for Mutant Alleles at the PHYA and PHYB Loci of Arabidopsis designations (Koornneef et al., 1980; Nagatani et al., 1993; Parks and Quail, New Designation Previous Designation Reference 1993; Reed et al., 1993; Whitelam et al., PhYA- 1 fhy2- 7 Whitelam et al. (1993) 1993), carry lesions in the structural genes phyA-2 fhy2-2 Whitelam et al. (1993) for phytochromes A or B (Dehesh et al., PhyA- 1O1 hy8- 1 Parks and Quail (1993); Dehesh et al. (1993) 1993; Reed et al., 1993, 1994; Whitelam PhyA-102 hy8-2 Parks and Quail (1993); Dehesh et al. (1993) et al., 1993) has focused attention on the PhyA- 103 hy8-3 Parks and Quail (1993); Dehesh et al. (1993) need for systematic allocation of mutant PhyA-201 frel-1 Nagatani et al. (1993); Reed et al. (1994) allele designations. PhyA-202 fre 1-2 Nagatani et al. (1993); Reed et al. (1994) In an attempt to encourage the use of phyA-203 m10 Reed et al. (1994) PhyA-204 Reed et al. (1994) a uniform phytochromenomenclature, we m20 PhyA-205 m26 Reed et al. (1994) propose adoption of the system summa- phyA-206 m34 Reed et al. (1994) rized in Table 1. The designations for PhyA-207 m35 Reed et al. (1994) wild-type and mutant genes, transcripts, PhyA-208 m36 Reed et al. (1994) and apoproteins are based on the estab- PhyA-209 Yl1 Reed et al. (1994) lished Arabidopsis nomenclature system PhyA-210 Y12 Reed et al. (1994) (National Science Foundation, 1993). The phyA-21 1 Yl8 Reed et al. (1994) symbols for the holoprotein and photo- chemical forms of phytochrome are logical hy3-BO64 Koornneef et al. (1980); Reed et al. (1993) extensions of existing abbreviations. In hy3-Vl97 Koornneef et al. (1980) hy3-d504 Koornneef et al. (1980) this convention, wild-type genes are in up- hy3-4- 1 1 7 Koornneef et al. (1980); Reed et al. (1993) percase italics, mutant alleles are in hy3-8-36 Koornneef et al. (1980); Reed et al. (1993) lowercase italics (in contrast to the bacteri- hy3-548 Koornneef et al. (1980); Reed et al. (1993) ally based system), the apoprotein (i.e., the hy3- 1053 Koornneef et al. (1980); Reed et al. (1993) polypeptide before chromophore attach- hy3-M4084 Koornneef et al. (1980); Reed et al. (1993) ment) is in uppercase roman, and the hy3-EMS142 Reed et al. (1993) holoprotein @e., mature, photoreversible hy3-464- 19 Reed et al. (1993) phytochrome after covalent chromophore attachment) is in lowercase roman. Where the subfamily identity has not been deter- extension of the Arabidopsis series (PHYE Physiologists (ASPP) (Briggs et al., 1993) mined or there is a need to refer generically PHYG, etc.). We recommend that the tem with regard to the holoprotein and pho- or collectively to all phytochromes, the “form” be reserved to describe the pho- tochemical forms. In an effort to resolve symbols PHY; phy, PHY mRNA, PHY, tochemical state of the phytochrome the ambiguity resulting from the inadver- phytochrome (or phy), Pr, and Pfr can be molecule (e.g., Pfr form of phytochrome tant publication of these two conflicting used without subfamily letter designations A) and that other terms, such as “type,” proposals, several of the authors of the to indicate wild-type genes, mutant genes, be used to describe the different gene ASPP Newsletter announcement (W.R.B., mRNA, apoprotein, holoprotein, and the products (e.g., type A phytochromes). J.C., R.P.H., E.S., W.m.).),after further dis- two photochemical forms of phytochrome, The proposed nomenclature system cussion, now endorse adoption of the respectively (Table 1). (Table 1) corresponds to that identified as present proposal (Table 1). This system appears to be sufficiently ‘Alternative phytochrome nomenclature” Three independently isolated sets of flexible to accommodate homologs of the in the appendix (labeled “4.2.8 Appendix”) Arabidopsis mutants, designated hy8 Arabidopsis genes from other plant spe- of a recent book chapter by Quail(l994). (Parks and Quail, 1993), fhy2 (Whitelam cies (e.g., maize PHYA, pea PHYB, etc.), The body of this book chapter contains et al., 1993), and frel (Nagatani et al., 1993) as well as potentially more divergent PHY another table identified simply as have been shown by molecular analysis sequences that do not fall readily into ex- “Phytochrome nomenclature,” which to be mutated in the PHYA gene (Dehesh isting subfamilies. In the latter case, the presents the original bacterial system- et al., 1993; Whitelam et al., 1993; Reed sequences might be designated either ac- based terminology that we now recom- et al., 1994). In accord with Arabidopsis cording to plant species, for those species mend be considered as superceded. The convention, these differently named mu- in which only asingle phytochrome gene present proposal is also different from that tants all represent phyA alleles. To has been detected (e.g., Ceratodon, Cer- published in a recent issue of the News- acknowledge this fact and to coordinate PHY [Thiimmler et al., 1992]), or by simple letter of the American Society of Plant the numbering of alleles, the three labora- 470 The Plant Cell

LETTER TO THE EDITOR

tories involved have agreed to adopt a Richard E. Kendrick Dehesh, K., Franci, C., Parks, B.M., Seeley, “100-series” numbering system according Department of Plant Physiology K.A., Short, T.W., Tepperman, J.M., and to the following: WhitelamlHarberd labo- Wageningen Agricultural University Quail, P.H. (1993). ArabidopsisHYB locus en- codes phytochrome A. Plant Cell 5, ratory, 1-99; Quail laboratory, 100-199; NL-6703 BD Wageningen 1081-1088. Chory laboratory, 200-299. This system The Netherlands Koornneef, M., Rolff, and Spruit, C. (1980). appears to be flexible enough both to ac- E., Genetic control of light-inhibited hypocotyl commodate multiple alleles from a single Maarten Koornneef elongation in Arabidopsis thaliana (L.)Heynh. laboratory and to expand to include alleles Department of Genetics Z. Pflanzenphysiol. 100, 147-160. from additional laboratories,with minimal Agricultural University McCormac, A.C., Whitelam, G.C., Boylan, potential for inadvertent duplication. Ta- NL-6703 HA Wageningen M.T., Quail, P.H., and Smith, H. (1992). Con- ble 2 shows the new allele designations The Netherlands trasting responses of etiolated and based on this system for each previously light-adapted seedlings to red:far-red ratio: reported mutant. Brian Parks Acomparison of wild type, mutant and trans- Members of the hy3 class of long Department of Plant Biology genic plants has revealed differential hypocotyl mutants, originally isolated by Ohio State University functions of members of the phytochrome Koornneef et al. (1980), have recently been Columbus, OH 43210 family. J. Plant Physiol. 140, 707-714. shown to carry lesions in the PHYB struc- McCormac, A.C., Wagner, D., Boylan, M.T., tural gene (Reed et al., 1993). Thus, the Robert A. Sharrock Quail, P.H., Smith, H., and Whitelam, G.C. (1993). Photoresponses of transgenic hy3 mutants are in factphy6 mutants. Sev- Biology Department Arabidopsis seedlings expressing introduced era1 alleles at the HY3 locus were Montana State University phytochrome B-encoding cDNAs: Evidence described in the original report (Koornneef Bozeman, MT 59717 that phytochrome A and phytochrome B have et al., 1980), and severa1 more were de- distinct photoregulatory functions. Plant J. scribed in the more recent screen (Reed Eberhard Schafer 4, 19-27. et al., 1993). The laboratories involved in lnstitute Biology II Nagatani, A., Reed, J.W., and Chory, J. (1993). these two studies have agreed to the University of Freiberg lsolation and initial characterization of renaming of the hy3 alleles as indicated 79104 Freiberg im Breisgau Arabidopsis mutants that are deficient in in Table 2. Germany phytochrome A. Plant Physiol. 102,269-277. Nationai Science Foundatlon. (1993).The Mul- Peter H. Quail William F. Thompson tinationalCoordinated Arabidopsis Thaliana Genome Research Project. ProgressReport: U.C. BerkeleylUSDA Plant Gene Department of Botany North Carolina State University Year Three (NSF 93-173). (Washington, DC: Expression Center National Science Foundation). Albany, CA 94710 Raleigh, NC 27695-7612 Parks, B.M., and Quail, P.H. (1993). hy8, a new Garry C. Whitelam class of Arabidopsis mutants deficient in func- Winslow R. Briggs tional phytochrome A. Plant Cell 5, 39-48. Department of Plant Biology Department of Botany University of Leicester Quail, P.H. (1991). Phytochrome: A light- Carnegie lnstitution of Washington activated molecular switch that regulates Leicester LE1 7RH Stanford, CA 94305-4170 plant gene expression. Annu. Rev. Genet. United Kingdom 25, 389-409. Joanne Chory Quail, RH. (1994). Phytochromegenesand their Plant Biology Laboratory expression. In Photomorphogenesisin Plants, The Salk lnstitute R.E. Kendrick and G.H.M. Kronenberg, eds San Diego, CA 92186-5800 REFERENCES (Dordrecht: Kluwer Academic Publishers), pp. 71-104. Roger P. Hangarter Reed, J.W., Nagpal, I?, Poole, D.S., Furuya, Department of Plant Biology Briggs, W., Chory, J., Furuya, M., Hangarter, M., and Chory, J. (1993). Mutations in the Ohio State University R., Schaefer, E., Thompson, W., Chrispeels, gene for the red/far-red light receptor phytochrome B alter cell elongation and phys- Columbus, OH 43210 M., and Larkins, B.A. (1993). Journal editors adopt new phytochromenomenclature. ASPP iological responsesthroughout Arabidopsis Newslett. 20 (6), 8. development. Plant Cell 5, 147-157. Nicholas P. Harberd Reed, J.W., Nagatani, A., Elich, T., Fagan, Cambridge Laboratory Clack, T., Mathews, S., and Sharrock, R.A. (1994). The phytochrome apoprotein family M., andChory, J. (1994). Phytochrome Aand John lnnes Center in Arabidopsis is encoded by five genes: The phytochrome B have overlapping but distinct Norwich NR4 7UJ sequences and expression of PHYD and functions in Arabidopsis development.Plant United Kingdom PHYE. Plant MOI. Biol., in press. Physiol., in press. April 1994 471

FROM THE EDITOR

Sage, L. C. (1992). Pigment of the Imagination: programme of crop improvement. Pho- Thiimmler, F., Dufner, M., Kreisl, P., and A History of Phytochrome Research. {San tochem. Photobiol. 56, 815-822. Dlttrlch, P. (1992). Molecular cloning of a nov- Diego, CA: Academic Press). el phytochrome gene of the moss Ceramdon Smiths H'g and Whitelam9G*C' purpumus which encoaes a putative light- Sharrock, R.A., and Quall, P.H. (1989). Nove1 Phytochrome, afamiiy of photoreceptorswith regulated,protein kinase, Plant Biol. phytochrome sequences in Arabidopsis multiple physiologicalroles. Plant Cell Envi- 1o03-10,7~ thaliana: Structure, evolution, and differential ron. 13, 695-707. expressionof a plant regulatory photoreceptor Whltelam, G.C., Johnson, E., Peng, J., Caro!, family. Genes Dev. 3, 1745-1757. Somem, D.E., Sharrock, R.A., Tepperman, P.,Andemn, M.L., Cowl, J.S., andHaWrd, J.M., and Quail, P.H. (1991). The hy3 long N.P. (1993). Phytochrome A null mutants of Smlth, H. (1992). The ecological functions of hypocotyl mutant of Arabidopsis is deficient Arabidopsis display a wildtype phenotype the phytochromefamily. Cluestoatransgenic in phytochrome B. Plant Cell 3, 1263-1274. in white light. Plant Cell 5, 757-768.

Still Having an lmpact

THE PLANT CELL is once again the plant lmpact factors tend to be remarkably continuing high impact factor of THE science journal whose articles are cited constant from year to year, and THE PLANT CELL. Although impact factor is most frequently, according to data com- PLANT CELL's are no exception: Our 1991 just one measure of the quality of a jour- piled by the lnstitute for Scientific impact factor (which was published in nal, we believe that the many citations to lnformation (ISI). ISI calculates citation 1992 and discussed in an editorial in the the articles published in THE PLANT rates by counting the number of citations November 1992 issue) was 8.58, and our CELL testify to their quality and influence, in a given year to articles published in a 1992 impact factor was recently deter- as well as to the interest they generate particular journal during the two previous mined to be 8.50. A different, lower figure both inside and outside the plant science years. Dividing this by the total number was printed in the 1992 Journal Citation community. of source articles published in the jour- Report and quoted by severa1 journals, nal, during those two years yields an but the ISI subsequently revised that fig- average citation rate known as the "im- ure after discovering that it had been Brian A. Larklna pact factor," which ISI publishes in its calculated incorrectly. Editor annual Journal Citation Report. We are pleased to be able to report the THE PLANT CELL