Nomenclature for Two-Component Signaling Elements of Rice

Plants make use of two-component systems for signal transduction, and these are involved in vital cellular processes such as the responses to cytokinins, ethylene, red/far-red light, and osmosensing (Schaller et al., 2002). Two-component systems were originally identified in bacteria, and in their simplest form involve a His kinase and a response regulator that participate in a phosphorelay (Mizuno, 1997). Of particular relevance to plants is a permutation on the two-component system known as the multistep phosphorelay, which incorporates an additional protein called a His-containing phosphotransfer protein into the phosphorelay (Schaller et al., 2002).

In plants, two-component signaling has been studied most extensively in the dicot Arabidopsis (Arabidopsis thaliana; Schaller et al., 2002). But in the past several years, as the rice (Oryza sativa) genome has been sequenced (Feng et al., 2002; Goff et al., 2002; Sasaki et al., 2002; Yu et al., 2002; Rice Chromosome 10 Sequencing Consortium, 2003; International Rice Genome Sequencing Program, 2005), publications have begun to appear on the two-component signaling elements of rice (Murakami et al., 2003; Doi et al., 2004; Han et al., 2004; Yau et al., 2004; Murakami et al., 2005; Ito and Kurata, 2006; Jain et al., 2006; Pareek et al., 2006). Given the broad impact that the two-component signaling systems have on plant growth and development, the number of publications describing their action in rice is likely to increase rapidly in the coming years. It is thus necessary that a uniform nomenclature be adopted to facilitate scientific communication.

Unfortunately, because publications on two-component signaling elements of rice appeared from multiple laboratories within a short period of time, it was not possible to coordinate the terminology being used. This resulted in multiple designations being applied to the same gene, different criteria being used for classifying genes into families, and some redundancy with previously used gene symbols. Now with a high-quality rice genome sequence available and most if not all of the two-component signaling elements identified, it is timely to implement a standardized nomenclature for the rice two-component signaling elements.

In assigning gene symbols, we followed the rules for gene symbols in rice adapted from the 1986 report of the Committee on Gene Symbolization, Nomenclature, and Linkage (the November 7, 2005 draft document is available at http://www.gramene.org/documentation/nomenclature/). Thus all gene symbols are given in italics with the first letter capitalized. Although not shown in the tables, the protein symbol should be identical to the adopted gene symbol, the only difference being that it is written using all uppercase characters in italics followed by the numeric locus identifier. Precedence of publication was the primary determinant of the gene symbol and, whenever possible, we used the same gene symbol for all related genes. Additional symbols for the same gene were assigned as synonyms. A rice designation (e.g. Os) is not part of the gene symbol but may be added when needed to differentiate between similar genes of other species.

Table I.

His kinase-like proteins of rice

Gene Symbol	Synonyms	Chromosome Locus	Featuresa	Family
Ers1b		Os03g49500	C2H4, HK	Ethylene receptor
Ers2b		Os05g06320	C2H4, HK	Ethylene receptor
Etr2b		Os04g08740	C2H4, HKL, Rec	Ethylene receptor
Etr3b		Os02g57530	C2H4, HKL, Rec	Ethylene receptor
Etr4b		Os07g15540	C2H4, HKL, Rec	Ethylene receptor
Hk1c		Os06g44410	HK, Rec	AtCKI2 like
Hk2c	Ohk1d	Os06g08450	HK, Rec	AtCKI1 like
Hk3c	Crl2e, Ohk2d	Os01g69920	CHASE, HK, Rec	Cytokinin receptor
Hk4c	Crl1be, Ohk4d	Os03g50860	CHASE, HK, Rec	Cytokinin receptor
Hk5c	Crl3e, Ohk3d	Os10g21810	CHASE, HK, Rec	Cytokinin receptor
Hk6c	Crl1ae, Ohk5d	Os02g50480	CHASE, HK, Rec	Cytokinin receptor

^aFeatures noted are conserved His-kinase domain (HK), diverged His-kinase-like domain (HKL), receiver domain (Rec), CHASE domain for cytokinin binding (CHASE), and ethylene-binding domain (C₂H₄).

^bYau et al. (2004).

^cPareek et al. (2006).

^dIto and Kurata (2006).

^eHan et al. (2004).

Table II.

His-containing phosphotransfer proteins of rice

Gene Symbol	Synonyms	Chromosome Locus	Featuresa
Ahp1	Hpt2b, Ohp1c	Os08g44350	HPt
Ahp2	Hpt3b, Ohp2c	Os09g39400	HPt
Php1	Hpt1b	Os01g54050	Pseudo-HPt
Php2	Hpt4b	Os05g09410	Pseudo-HPt
Php3	Hpt5b	Os05g44570	Pseudo-HPt

^aFeatures indicate whether the proteins contain a conserved His-containing phosphotransfer domain (HPt) or a pseudo-HPt lacking the His that is phosphorylated.

^bPareek et al. (2006).

^cIto and Kurata (2006).

Table III.

Response regulators of rice

Gene Symbol	Synonyms	Chromosome Locus	Featuresa	Family
Rr1b	Rra9c	Os04g36070	Rec	Type A
Rr2b	Rra10c	Os02g35180	Rec	Type A
Rr3b	Rra7c	Os02g58350	Rec	Type A
Rr4b	Rra3c	Os01g72330	Rec	Type A
Rr5b	Rra4c	Os04g44280	Rec	Type A
Rr6b	Rra6c	Os04g57720	Rec	Type A
Rr7b	Rra5c	Os07g26720	Rec	Type A
Rr8b	Rra13c	Os08g28900	Rec	Type A
Rr9b	Rra1c	Os11g04720	Rec	Type A
Rr10b	Rra2c	Os12g04500	Rec	Type A
Rr11d	Rra8c	Os02g42060	Rec	Type A
Rr12d	Rra11c	Os08g28950	Rec	Type A
Rr13d	Rra12c	Os08g26990	Rec	Type A
Rr21	Rrb1c, Orr1d	Os03g12350	Rec, Myb	Type B
Rr22	Rrb4c, Orr2d	Os06g08440	Rec, Myb	Type B
Rr23	Rrb5c, Orr3d	Os02g55320	Rec, Myb	Type B
Rr24	Rrb2c, Orr4d	Os02g08500	Rec, Myb	Type B
Rr25	Rrb3c, Orr5d	Os06g43910	Rec, Myb	Type B
Rr26	Rrb6c, Orr6d	Os01g67770	Rec, Myb	Type B
Rr27	Rra16c	Os05g32880	Rec, Myb	Type B
Rr28	Rra22c	Os04g28160	Rec, Myb	Type B
Rr29	Rrb7c	Os04g28130	Rec, Myb	Type B
Rr30	Ehd1e	Os10g32600	Rec, Myb	Type B
Rr31		Os08g35650	Rec, Myb	Type B
Rr32		Os08g17760	Rec, Myb	Type B
Rr33	Rra19c	Os08g35670	Rec, Myb	Type B
Rr41	Rra14c	Os03g53100	Rec	Type C
Rr42	Rra15c	Os04g13480	Rec	Type C
Prr1f		Os02g40510	Rec(D-E), CCT	Clock
Prr37f	Prr4c	Os07g49460	Rec(D-E), CCT	Clock
Prr73f	Prr3c	Os03g17570	Rec(D-E), CCT	Clock
Prr59f	Prr5c	Os11g05930	Rec(D-E), CCT	Clock
Prr95f	Prr2c	Os09g36220	Rec(D-E), CCT	Clock
Prr10	Rra18c	Os05g32890	Rec(D-E), Myb
Prr11		Os04g28150	Rec(D-E)
Prr12	Rra17c	Os04g28120	Rec(D-A)

^aFeatures include receiver domain (REC) with change in phosphorylated Asp indicated if differing from the conserved sequence, Myb-like DNA-binding domain (Myb), and CCT motif found in clock proteins.

^bJain et al. (2006).

^cPareek et al. (2006).

^dIto and Kurata (2006).

^eDoi et al. (2004).

^fMurakami et al. (2003).

For the His kinases, the ethylene receptor family retains the original designations from Yau et al. (2004), which are consistent with gene symbols used in other plant species. The other rice His kinases use the gene symbol Hk, including the four members of the cytokinin receptor family (Pareek et al., 2006).

The His-containing phosphotransfer proteins are given the gene symbol Ahp (authentic His-containing phosphotransfer protein) if they contain the conserved His residue that is phosphorylated, and the gene symbol Php (pseudo His-containing phosphotransfer protein) if they lack the conserved His. These new symbols are in accordance with nomenclature for genes encoding response regulators (see below), and will simplify discussion of the His-containing phosphotransfer proteins because the symbols carry information related to function.

The rice response regulators are given the gene symbol Rr if they contain the conserved Asp that serves as the phosphorylation site (Jain et al., 2006), and the gene symbol Prr if they lack the conserved Asp (Murakami et al., 2003). The rice response regulators are numbered according to type (the gene symbols for type A starting from Rr1, type B starting from Rr21, and type C starting from Rr41), such that if additional response regulators of each type are found in annotation of the genome, they may still be numbered in sequence with their more closely related sequences. Note that we are using the same definition of the type A response regulators as that employed for Arabidopsis (short N- and C-terminal extensions in addition to the receiver domain, related at the sequence level based on phylogenetic analysis, and induced by cytokinin). The type B response regulators are transcriptional regulators with C-terminal extensions containing a Myb-like DNA-binding domain, although it should be pointed out that there is substantial sequence variation among the rice Myb-like motifs. We also introduce the term type C response regulator to refer to OsRr41 and 42 (along with AtARR22 and 24) which, although the proteins lack long C-terminal extensions, are not closely related to the type A response regulators based on phylogenetic analysis (Schaller et al., 2002).