Discovery of genes affecting resistance of barley to adapted and non-adapted powdery mildew fungi

Douchkov, Dimitar; Lück, Stefanie; Johrde, Annika; Nowara, Daniela; Himmelbach, Axel; Rajaraman, Jeyaraman; Stein, Nils; Sharma, Rajiv; Kilian, Benjamin; Schweizer, Patrick

doi:10.1186/s13059-014-0518-8

Table 4 Barley candidate genes with a high score of converging evidence for a role in QR to Bgh

From: Discovery of genes affecting resistance of barley to adapted and non-adapted powdery mildew fungi

U35-contig no. ^a	CG no.	Proposed function (BlastX)	Functional category	Chr ^b	Position (cM) ^b	Linkage map ^b	Transcript regul. epidermis	Transcript regul. leaf	Rel. SI (%) ^c	TIGS or OEX	Transcr. regul.	CNV	Colocal Meta- QTL ^d	Ass_SNP_ hapl_ GWAS	CE score ^e
964	1	BAX-Inhibitor1	Cell & death	6H	51.6	Marcel_09_int	UP	UP	41.9	2	2	1	0	0	5
3589	2	Hv-Lsd1a	Cell & death	5H	43.1	BOPA_cons	NS	NS	49.9	2	0	1	1	1	5
16561	3	Hv-Mlo	Cell & death	4H	103.1	BOPA_cons	UP	UP	13.8	2	2	0	1	0	5
16942	4	Stomatin-like protein (Rnr10)	Cell & death	5H	44.2	9K_WGS_BxM	UP	UP	62.5	1	2	0	1	0	4
11820	5	AP2-EREBP transcription factor	Gene expr.	7H	120.4	9K_WGS_BxM	UP	-	39.0	2	2	0	0	-	4
15932	6	Hv-WRKY2	Gene expr.	7H	126.3	9K_WGS_BxM	UP	UP	44.6	1	2	0	0	1	4
383	7	Hv-WRKY21	Gene expr.	3H	54.4	BOPA_cons	NS	DOWN	41.5	2	1	0	1	-	4
4162	8	Hv-WRKY28	Gene expr.	5H	46.5	9K_WGS_BxM	UP	UP	56.7	2	2	0	0	0	4
43536	9	Hv-WRKY45	Gene expr.	3H	59.3	9K_WGS_BxM	UP	UP	39.4	2	2	0	1	-	5
2987	10	Os-WRKY68-like	Gene expr.	2H	92.3	9K_WGS_BxM	UP	NS	35.7	2	2	0	0	1	5
2705	11	Pre-mRNA splicing factor PRP38	Gene expr.	7H	33.0	Marcel_09_int	UP	NS	79.4	1	2	0	1	0	4
16863	12	6-Phosphogluconolactonase 2	Prim. metab.	2H	56.3	BOPA_cons	DOWN	DOWN	142.9	1	2	0	1	-	4
604	13	Alpha/beta hydrolase	Prim. metab.	4H	126.1	Marcel_09_int	UP	UP	72.2	0	2	0	1	1	4
5070	14	Short chain dehydrogen/reductase	Prim. metab.	5H	41.6	9K_WGS_BxM	DOWN	DOWN	173.9	0	2	1	1	-	4
15523	15	Stearoyl-ACP desaturase	Prim. metab.	2H	58.1	9K_WGS_BxM	UP	UP	78.5	0	2	1	1	-	4
3071	16	ARM repeat protein (Rnr5)	Protein	3H	95.4	BOPA_cons	UP	UP	49.0	2	2	1	0	0	5
17055	17	Nucellin-like aspartic protease	Protein	4H	48.5	BOPA_cons	UP	UP	41.4	1	2	0	1	0	4
19087	18	Subtilisin-like serine proteinase	Protein	3H	47.1	9K_WGS_BxM	UP	UP	137.4	2	2	0	1	-	5
13715	19	Ubiquitin	Protein	7H	104.1	9K_WGS_BxM	UP	NS	427.9	2	2	1	0	-	5
13712	20	Ubiquitin	Protein	5H	50.3	BOPA_cons	NS	NS	270.3	2	0	1	1	-	4
1746	21	4-Coumarate coenzyme A ligase	Sec. metab.	6H	59.8	Marcel_09_int	UP	UP	177.8	2	2	0	0	0	4
14914	22	Caffeic acid 3-O-methyltransferase	Sec. metab.	2H	89.9	Marcel_09_int	UP	UP	42.5	1	2	1	0	0	4
2091	23	Chorismate Synthase	Sec. metab.	4H	55.3	9K_WGS_BxM	UP	UP	72^f	2	2	0	1	1	6
14239	24	Phenylalanine ammonia-lyase	Sec. metab.	2H	77.1	Marcel_09_int	UP	UP	95.5	0	2	1	1	-	4
14693	25	Calreticulin 1 or 2^g	Secr. & CW	2H	151.4	BOPA_cons	UP	UP	101.9	1	2	0	1	1	5
17745	26	Golgi nucl.-sugar transporter	Secr. & CW	4H	65.8	9 K_WGS_BxM	UP	UP	56.5	2	2	0	0	-	4
6978	27	Hv-CslA11	Secr. & CW	3H	143.0	9 K_WGS_BxM	DOWN	DOWN	145.9	2	2	0	1	-	5
17157	28	Hv-CslD2 (Rnr6)	Secr. & CW	7H	3.8	9 K_WGS_BxM	UP	UP	216.3	2	2	1	1	0	6
14954	29	Hv-Ger4d (SOD)	Secr. & CW	4H	119.8	BOPA_cons	UP	UP	149.0	2	2	1	1	0	6
16280	30	Hv-Ger5a (SOD)	Secr. & CW	5H	97.4	Marcel_09_int	UP	NS	61.0	2	2	0	0	-	4
14157	31	Hv-Prx40	Secr. & CW	3H	81.2	Marcel_09_int	UP	UP	184.1	2	2	1	0	0	5
14158	32	Hv-Prx64	Secr. & CW	3H	81.2	Marcel_09_int	UP	UP	113.7	1	2	0	0	1	4
4293	33	Hv-SNAP34 (Rnr3)	Secr. & CW	2H	63.6	Marcel_09_int	UP	UP	179.8	2	2	0	1	0	5
16316	34	Diacylglycerol kinase	Signaling	2H	140.3	BOPA_cons	UP	UP	40.2	2	2	1	0	0	5
39894	35	Disease resistance protein Hcr2-0B	Signaling	-	-	-	UP	-	122.4	2	2	1	-	-	5
1818	36	OPDA reductase	Signaling	2H	64.2	BOPA_cons	UP	UP	68.8	0	2	0	1	1	4
15506	37	Receptor-like kinase (BAK-1)	Signaling	3H	142.7	Marcel_09_int	UP	UP	71.2^f	2	2	0	0	0	4
18640	38	Receptor-like kinase (DUF26)	Signaling	5H	167.6	9 K_WGS_BxM	UP	UP	48.2	1	2	0	0	1	4
10720	39	Receptor-like kinase (DUF26)	Signaling	-	-	-	NS	UP	23.3	2	1	1	-	-	4
5850	40	Receptor-like kinase (lectin-like)	Signaling	5H	46.2	BOPA_cons	UP	UP	78.2	0	2	1	1	1	5
20697	41	Receptor-like kinase (lectin-like)	Signaling	7H	44.4	9 K_WGS_BxM	UP	UP	45.4	2	2	1	0	-	5
20304	42	Receptor-like kinase (lectin-like)	Signaling	2H	59.2	ZIPPER	UP	UP	60.5	0	2	1	1	-	4
26360	43	Receptor-like kinase (lectin-like)	Signaling	5H	46.2	CAPS_BxM	UP	NS	66.7	0	2	1	1	0	4
39885	44	Receptor-like kinase (LRR)	Signaling	-	-	-	NS	UP	32.6	2	1	1	-	-	4
16135	45	Triticum aestivum kinase (TAK)	Signaling	3H	6.8	9 K_WGS_BxM	NS	UP	52.1	2	1	1	0	-	4
16558	46	Glutathione S-transferase	Stress	4H	96.6	BOPA_cons	COMPL.	UP	101.2	0	2	1	1	0	4
1285	47	Sugar transporter (Os-SWEET2a)	Transport	1H	18.1	BOPA_cons	COMPL.	NS	40.8	1	2	0	1	0	4
2230	48	Charged MVB protein 5	Unknown	1H	0.2	9 K_WGS_BxM	UP	UP	86.7	0	2	1	1	-	4
14824	49	Hv-Ger2a	Unknown	2H	44.6	Marcel_09_int	DOWN	DOWN	58.4^f	2	2	0	0	0	4
19741	50	Unknown protein	Unknown	7H	23.0	Marcel_09_int	UP	UP	51.8	2	2	1	1	0	6
1681	51	Unknown protein	Unknown	2H	136.2	Marcel_09_int	UP	UP	66.4	1	2	1	0	1	5

^aHarvEST database.
^bMap position derived from different mapping populations: 9 K_WGS_BxM, Barke x Morex population for Illumina 9 K SNP chip and WGS contig anchoring by POPSEQ; BOPA_cons, Barley OPA123-2008, consensus map for barley SNP genotyping deposited in GrainGenes database; CAPS_IxF, CAPS marker-based mapping in Igri x Franka DH population (Schweizer lab); Marcel_09_int, Consensus map, Barley, Integrated, Marcel 2009 deposited in GrainGenes database; ZIPPER, gene-order based map position using stringent sequence homology scores between cereal species.
^cRelative susceptibility index caused by TIGS or transient over-expression, normalized to corresponding empty-vector controls.
^dMap position lying between outmost flanking markers of meta-QTL (consisting of ≥3 overlapping QTL) for resistance to Bgh.
^eSum of scores assigned for: (1) TIGS or transient over-expression effect, (2) transcript regulation either in leaf epidermis or entire leaves, (3) significant copy number variation (CNV), (4) meta-QTL co-localization, and (5) SNP or haplotype association with QR to Bgh. More weight (2 CE scores) was assigned to significant TIGS or OEx effects after false-discovery correction (FDR 0.1), and to transcript regulation in the leaf epidermis (versus regulation in entire leaf samples).
^fEffect of transient over-expression.
^gAlso regulates Ca²⁺ concentrations and is therefore also involved in signaling.
Ass, marker-trait association of SNP and/or gene haplotype in a candidate-gene approach or by genome-wide association (GWAS) analysis; Chr, chromosome; CE, convergent evidence; cM, centimorgan; CW, cell wall; expr., expression; metab., metabolism; prim, primary; sec., secondary; secr., secretion; SI, susceptibility index.
A more detailed discussion of individual candidate genes can be found in Additional file 6 provided online.

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