The Arabidopsis CDPK-SnRK superfamily of protein kinases

Abstract

The CDPK-SnRK superfamily consists of seven types of serine-threonine protein kinases: calcium-dependent protein kinase (CDPKs), CDPK-related kinases (CRKs), phosphoenolpyruvate carboxylase kinases (PPCKs), PEP carboxylase kinase-related kinases (PEPRKs), calmodulin-dependent protein kinases (CaMKs), calcium and calmodulin-dependent protein kinases (CCaMKs), and SnRKs. Within this superfamily, individual isoforms and subfamilies contain distinct regulatory domains, subcellular targeting information, and substrate specificities. Our analysis of the Arabidopsis genome identified 34 CDPKs, eight CRKs, two PPCKs, two PEPRKs, and 38 SnRKs. No definitive examples were found for a CCaMK similar to those previously identified in lily (Lilium longiflorum) and tobacco (Nicotiana tabacum) or for a CaMK similar to those in animals or yeast. CDPKs are present in plants and a specific subgroup of protists, but CRKs, PPCKs, PEPRKs, and two of the SnRK subgroups have been found only in plants. CDPKs and at least one SnRK have been implicated in decoding calcium signals in Arabidopsis. Analysis of intron placements supports the hypothesis that CDPKs, CRKs, PPCKs and PEPRKs have a common evolutionary origin; however there are no conserved intron positions between these kinases and the SnRK subgroup. CDPKs and SnRKs are found on all five Arabidopsis chromosomes. The presence of closely related kinases in regions of the genome known to have arisen by genome duplication indicates that these kinases probably arose by divergence from common ancestors. The PlantsP database provides a resource of continuously updated information on protein kinases from Arabidopsis and other plants.

Figure 1.

Diagrammatic representation of the domain structures of protein kinases in the CDPK-SnRK superfamily. The domains are described in more detail in the text. Broken lines at N or C termini indicate regions of variable length and function. Calcium-binding EF hands are indicated as black boxes, whereas corresponding regions in related protein kinases that lack consensus EF hand sequences are depicted in gray. The C in the autoinhibitor domain of CaMK and CCaMK indicates that the autoinhibitor domain of this kinase overlaps with a calmodulin-binding domain. The SnRK1 C-terminal domain regulatory domain is indicated by dashed lines. D/E is the acidic patch found in the SnRK2 group while the autoinhibitor (NAF/FISL) domain of the SnRK3 group is hatched.

Figure 2.

Sequence tree for the Arabidopsis CDPK/SnRK superfamily based on alignment of kinase catalytic domains. The five kinase groups (CDPK, CRK, PPCK, PEPRK, and SnRK) are delimited by dark gray blocks. Subgroups within the CDPK and SnRK groups are shown as lighter shaded blocks. Non-Arabidopsis sequences included as outgroups are followed by sequence identifiers and are shown in italics and with dashed lines. CAPK denotes bovine cAMP-dependent protein kinase. Abbreviations for other organisms are: Sc, Brewer's yeast; Dm, fruitfly (Drosophila melanogaster); Md, apple (Malus domestica); Nt, tobacco (Nicotiana tabacum); Ll, Lilium longiflorum; Rn, Rattus norvegicus; Sp, fission yeast (Schizosac-charomyces pombe); Et, Eimeria tenella (apicomplexan); Pf, Plasmodium falciparum (apicomplexan); Bn, canola (Brassica napus); Kf, Kalanchoe fedtschenkoi; Mc, common ice plant (Mesembryanthemum crystallinum); Le, tomato (Lycopersicon esculentum); Os, rice (Oryza sativa); and Ma, Musa acuminata. Bootstrap supports for specific branches are shown in color. Noncolored branches are supported by greater than 800 trees in 1,000 bootstrap trials.

Figure 3.

Intron positions in Arabidopsis CDPKs, CRKs, PPCKs, PEPRKs, and SnRKs. Kinases are diagrammed as rectangles; N, N terminus; C, C terminus; Roman numerals, conserved kinase domains (Hanks and Hunter, 1995); J, junction domain; 1–4, EF hands; D/E, acidic patch. Introns are represented by triangles that contain a number indicating the phase of the intron: 0 = intron inserted between intact codons; 1 = intron inserted after first nucleotide of a codon; 2 = intron inserted after second nucleotide of a codon. White triangles are introns conserved in all members of a group, whereas gray-filled introns are only found in some members of the group. Dotted lines connect introns at comparable positions in different kinase groups. A, Intron positions in CPKs, CRK, PPCKs, and PEPRKs. B, Intron positions in SnRKs.

Figure 4.

Chromosome positions of CDPK, CRK, PPCK, and PEPRK genes. The positions of CDPKs are shown to the left of each chromosome, whereas the CRKs, PPCKs, and PEPRKs are indicated on the right. Values in parentheses are distances in megabases.

Figure 5.

Chromosome positions of SnRK genes. Values in parentheses are distances in megabases.