The minimal kinome of Giardia lamblia illuminates early kinase evolution and unique parasite biology

Manning, Gerard; Reiner, David S; Lauwaet, Tineke; Dacre, Michael; Smith, Alias; Zhai, Yufeng; Svard, Staffan; Gillin, Frances D

doi:10.1186/gb-2011-12-7-r66

Table 2 Summary of Giardia kinome classification

From: The minimal kinome of Giardia lamblia illuminates early kinase evolution and unique parasite biology

Group	Family	Subfamily	Count	ORF ID	Notes
Primordial kinases in *Giardia*strain WB (core kinome plus Nek1)
AGC	Akt		1	11364	Metabolic rate control
AGC	NDR	NDR-unclassified	2	8587, novel	Mitotic exit, morphology, centrosomes
AGC	PDK1		1	113522	Lipid signaling, AGC master kinase
AGC	PKA		2	11214, 86444	cAMP responsive kinase
AGC	PTF	FPK	1	221692	Potential flippase kinase
CAMK	CAMK1		1	11178	Calcium-dependent signaling
CAMK	CAMKL	AMPK	3	14364, 16034, 17566	Energy metabolism
CK1	CK1	CK1-D	1	7537	Absent from ciliates and plants
CMGC	CDK	CDC2	3	15397, 8037, 9422	Master kinase of cell cycle
CMGC	CDK	CDK5	1	16802	Non-cell cycle CDK
CMGC	CDKL		1	96616	Functions unknown
CMGC	CK2		1	27520	Diverse functions, hundreds of substrates
CMGC	CLK		1	92741	Splicing and other functions
CMGC	DYRK	DYRK1	1	101850	Not in ciliates, Trichomonas, or moss
CMGC	DYRK	DYRK2	3	137695, 17417, 17558	Varied functions
CMGC	GSK		2	17625, 9116	Glycogen synthase kinase 3. Diverse functions
CMGC	MAPK	ERK1	1	17563	Canonical MAPK pathway
CMGC	MAPK	ERK7	1	22850	Variant MAPK gene
CMGC	RCK	MAK	2	14172, 6700	Meiosis, flagella
CMGC	RCK	MOK	1	14004	Flagellar regulation
CMGC	SRPK		1	17335	Splicing
Other	Aur		1	5358	Mitotic kinase
Other	Bud32		1	16796	Telomere associated (KEOPS complex)
Other	CAMKK		1	96363	CAMK kinase
Other	CDC7		1	112076	Cell cycle
Other	IKS		1	137730	Not in ciliates or moss
Other	NAK	NAK-unclassified	2	12223, 2583	Varied functions
Other	NEK	NEK1	1	137719	Flagellar and centrosomal functions. Only Nek with clear non-excavate orthologs
Other	PEK	GCN2	1	12089	Response to amino acid starvation
Other	PLK	PLK1	1	104150	Mitotic kinase. Lost in plants
Other	SCY1		1	8805	Cryptic functions
Other	TTK		1	4405	Not in ciliates or moss
Other	ULK	Fused	1	17368	Varied functions
Other	ULK	ULK	1	103838	Autophagy
Other	Uni1		1	16436	Uncharacterized. Lost in plants, fungi, animals
Other	VPS15		1	113456	Vesicular transport, autophagy
Other	WEE	WEE-unclassified	1	115572	Key cell cycle kinase
Other	WNK		1	90343	Osmotic balance
PKL	PIK	FRAP	1	35180	Metabolic rate control (mTOR/TOR)
PKL	PIK	PIK-unclassified	1	16805	Weakly similar to ATR, but may be a lipid kinase
PKL	RIO	RIO1	1	17449	Ribosome biogenesis
PKL	RIO	RIO2	1	5811	Ribosome biogenesis
STE	STE11	CDC15	2	16834, 6199	Functions in mitotic exit; lost in plants and holozoans
STE	STE11	STE11-unclassified	1	1656	MAP kinase kinase kinase
STE	STE20	FRAY	1	10609	Not in ciliates, usually co-occurs with Wnk
STE	STE20	MST	1	15514	NDR kinase
STE	STE20	PAKA	1	2796	Transduces membrane signaling from small GTPases
STE	STE20	YSK	1	14436	Universal STE20 kinase
STE	STE7	MEK1	1	22165	MAP kinase kinase
*Giardia* -specific classes and unique kinases
Other	Nek	Nek-GL1	11	Table S1^a
Other	Nek	Nek-GL2	3	Table S1^a
Other	Nek	Nek-GL3	4	Table S1^a
Other	Nek	Nek-GL4	32	Table S1^a
Other	Nek	Nek-Unclassified	147	Table S1^a
CMGC	CMGC-GL1		2	17139, 21116	Divergent pair of CMGC-like kinases
Other	Other-GL1		3	17392, 17378, 6624	Trio of kinases with no specific homologs
Other	Other-unique		8	Table S1^a	Kinases with no specific homologs
CMGC	CDK	CDK-unclassified	3	11290, 4191, 14578	Divergent cyclin-dependent kinase
CAMK	CAMK-unique		1	13852	Divergent CAMK group member
CAMK	CAMKL	CAMKL-unclassified	2	14661, 9487	Divergent CAMKL family member
Non-protein kinases from PKL
PKL	CAK	ChoK	1	4596	Choline and aminoglycoside kinase
PKL	CAK	FruK	1	2969	Fructosamine kinase
PKL	PIK	PI3K	2	14855, 17406	Phosphatidyl inositol 3' kinase
PKL	PIK	PI4K	1	16558	Phosphatidyl inositol 4' kinase
Basal kinases found in *Trichomonas* , but not *Giardia*
AGC	MAST	MAST			Microtubule-associated serine kinases. Lost in fungi
Atypical	TAF1				Basal transcriptional machinery, TFIID subunit
CAMK	CDPK				Calcium-dependent protein kinase. Lost from unikonts
CK1	TTBK				Tau tubulin kinase. Found in unikonts, some chromalveolates, and excavates
CMGC	CDK	CDK7			Transcription initiation and DNA repair: subunit of TFIIH
CMGC	CDK	CDK12 (CRK7)			Phosphorylates CTD of RNA polymerase II
CMGC	DYRK	YAK			Lost in metazoans. Possible function in splicing
Other	TLK				DNA break repair. Lost in fungi, Dictyostelium
PKL	PIK	ATM			DNA break repair
PKL	PIK	ATR			DNA break repair
CMGC	CDK	CDK20 (CCRK)			Cilium-associated, CDK-activating kinase. Found in unikonts, algae, and Trichomonas
TKL					Diverse group related to tyrosine kinases
Basal kinases found in *Leishmania* but not *Giardia* or *Trichomonas*
PKL	ABC1	ABC1-A			Mitochondrial kinase
PKL	ABC1	ABC1-B			Mitochondrial kinase
PKL	ABC1	ABC1-C			Mitochondrial kinase
HisK	PDHK	BCKDK			Mitochondrial kinase
HisK	PDHK	PDHK			Mitochondrial kinase
CMGC	DYRK	DYRKP			Splicing? Also lost in animals, fungi, Dictyostelium
PKL	PIK	DNAPK			DNA break repair. Absent from fungi, nematodes, insects, some plants
Basal kinases not found in excavates
Other	IRE				Endoplasmic reticulum unfolded protein response
Other	PEK	PEK			Endoplasmic reticulum unfolded protein response. Absent from ciliates
Other	NAK	MPSK			Secretory pathway function. Absent from ciliates
Other	BUB				Mitotic spindle checkpoint. Absent from ciliates
CMGC	CDK	CDK8			Phosphorylates CTD of RNA polymerase II
CMGC	CDK	CDK11			Mitotic spindle function? Absent from fungi
CMGC	DYRK	PRP4			Splicing. Lost in fungi
PKL	PIK	SMG1			Nonsense-mediated decay of spliced transcripts. Absent from ciliates
HisK	HisK				Histidine kinases. Absent from metazoans
PKL	Alpha	VWL			Functions unknown. Absent from metazoans
AGC	PKG				cGMP-activated protein kinase. Absent from fungi, Dictyostelium
PKL	ABC1	ABC1-D			Mitochondrial kinase. Absent from ciliates
Atypical	G11				Function unknown. Absent from ciliates
Other	PLK	SAK			Mitotic kinase. Absent from plants
Other	Haspin				Functions in mitosis. Absent from ciliates
AGC	RSK				Ribosomal S6 kinase. Excavates lack conserved substrates sites in tail of ribosomal protein S6
CAMK	CAMKL	MARK			Microtubule affinity-regulating kinase. Absent from plants
Other kinases shared between excavates and one other ancient group
CAMK	CAMKL	LKB			Activator of other CAMKL kinases. Found in excavates and unikonts, lost in Giardia and L. major
CAMK	CAMKL	CIPK	1	16235	Found in plants and excavates. CBL-interacting protein kinases
CK1	CK1	CK1y			Found in plants and Trichomonas

^aSee Additional file 1 for details. BCKDK, branched chain ketoacid dehydrogenase kinase; mTOR, mammalian target of rapamycin; PDHK, pyruvate dehydrogenase kinase; RSK, ribosomal S6 kinase; TLK, Tousled-like kinase; TOR, target of rapamycin. See Additional file 4 for definitions of other proteins.

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