Genome-wide Identification and Expression Analysis of the GRAS Gene Family in Response to Cold Stress in Chrysanthemum nankingense

doi:10.16420/j.issn.0513-353x.2021-1238

Acta Horticulturae Sinica ›› 2023, Vol. 50 ›› Issue (4): 815-830.doi: 10.16420/j.issn.0513-353x.2021-1238

• Research Papers • Previous Articles Next Articles

Genome-wide Identification and Expression Analysis of the GRAS Gene Family in Response to Cold Stress in Chrysanthemum nankingense

WANG Tonghuan¹, WU Yuxin¹, WU Yiyuan¹, LI Xinxin¹, LIU Mengyang¹, YANG Lianlian¹^,², LI Jiapeng¹^,², ZHANG Zhongshan¹^,², CAO Fang¹, ZHONG Xueting¹^,², WANG Zhanqi¹^,²^,^*()

1. College of Life Sciences，Huzhou University，Huzhou，Zhejiang 313000，China
2. Key Laboratory of Vector Biology and Pathogen Control of Zhejiang Province，Huzhou University，Huzhou，Zhejiang 313000，China

Received:2022-08-13 Revised:2022-12-11 Online:2023-04-25 Published:2023-04-27
Contact: *（E-mail：zhqwang@zjhu.edu.cn）

Abstract

Abstract:

In this study，the GRAS gene family of Chrysanthemum nankingense was identified by bioinformatics. Furthermore，the expression of CnGRAS gene family in response to low temperature stress was analyzed using the published RNA-Seq data. The results showed that the CnGRAS gene family consists of 80 members，which can be divided into 10 subfamilies；and the gene structures and protein domains were highly conserved between each member of the same subfamily. Replication evolution analysis showed that there was only tandem repeat in replication patterns of the CnGRAS gene family. A tissue-specific expression pattern of the CnGRAS gene family was observed in C. nankingense，and most of them were highly expressed in roots and leaves. GO enrichment analysis indicated that most of the CnGRAS gene family members were mainly located in the nucleus，which have a variety of molecular functions and participate in many biological processes. RNA-Seq data analysis showed that 14 CnGRAS genes were differentially expressed under at least one type of cold stress（short-term cold or long-term cold），and the CnGRAS32，CnGRAS33，CnGRAS40，CnGRAS44，CnGRAS56，CnGRAS74 and CnGRAS79 were significantly up-regulated under both short-term or long-term cold stress，indicating that these genes may play an essential role in C. nankingense in response to cold stress.

Key words: Chrysanthemum nankingense, GRAS, transcription factor, cold stress, expression analysis

CLC Number:

S644.9

WANG Tonghuan, WU Yuxin, WU Yiyuan, LI Xinxin, LIU Mengyang, YANG Lianlian, LI Jiapeng, ZHANG Zhongshan, CAO Fang, ZHONG Xueting, WANG Zhanqi. Genome-wide Identification and Expression Analysis of the GRAS Gene Family in Response to Cold Stress in Chrysanthemum nankingense[J]. Acta Horticulturae Sinica, 2023, 50(4): 815-830.

Figures/Tables 9

References 47

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基因名 Gene name	基因ID Gene ID	方向 Strand	开放阅读框/bp ORF	外显子数 Number of exons	蛋白质/aa Protein	等电点 pI	分子量/kD MW
CnGRAS1	CHR00004937-RA	反向 Reverse	1 401	6	466	4.6	52.8
CnGRAS2	CHR00004939-RA	反向 Reverse	948	6	315	4.5	35.8
CnGRAS3	CHR00004941-RA	反向 Reverse	1 305	4	434	4.6	48.9
CnGRAS4	CHR00004943-RA	反向 Reverse	1 005	5	334	5.0	37.9
CnGRAS5	CHR00010605-RA	反向 Reverse	1 464	3	487	5.7	54.8
CnGRAS6	CHR00010606-RA	反向 Reverse	1 551	6	516	5.5	57.9
CnGRAS7	CHR00030831-RA	反向 Reverse	1 317	6	438	5.3	49.3
CnGRAS8	CHR00009270-RA	反向 Reverse	882	3	293	5.2	33.7
CnGRAS9	CHR00003961-RA	反向 Reverse	3 216	3	1 071	5.5	121.1
CnGRAS10	CHR00055273-RA	反向 Reverse	762	4	253	5.7	28.5
CnGRAS11	CHR00032218-RA	反向 Reverse	1 407	2	468	6.1	52.6
CnGRAS12	CHR00031862-RA	正向 Forward	624	3	207	8.9	22.7
CnGRAS13	CHR00060013-RA	正向 Forward	2 187	7	728	5.1	81.5
CnGRAS14	CHR00049603-RA	反向 Reverse	1 965	3	654	5.5	71.8
CnGRAS15	CHR00044507-RA	正向 Forward	1 587	2	528	5.9	59.0
CnGRAS16	CHR00088841-RA	正向 Forward	684	2	227	6.4	25.3
CnGRAS17	CHR00057450-RA	反向 Reverse	1 809	4	602	6.4	66.5
CnGRAS18	CHR00032070-RA	正向 Forward	1 605	4	534	5.8	61.0
CnGRAS19	CHR00001839-RA	正向 Forward	1 656	1	551	6.2	62.0
CnGRAS20	CHR00003428-RA	正向 Forward	1 560	3	519	4.9	58.8
CnGRAS21	CHR00080196-RA	反向 Reverse	1 863	4	620	5.8	69.5
CnGRAS22	CHR00056344-RA	反向 Reverse	1 509	5	502	5.2	56.5
CnGRAS23	CHR00043261-RA	反向 Reverse	1 617	6	538	5.4	61.0
CnGRAS24	CHR00007360-RA	正向 Forward	1 647	6	548	5.7	61.3
CnGRAS25	CHR00084234-RA	反向 Reverse	1 971	5	656	6.3	75.5
CnGRAS26	CHR00026458-RA	正向 Forward	1 587	7	528	5.1	59.7
CnGRAS27	CHR00012285-RA	正向 Forward	1 392	5	463	5.8	53.1
CnGRAS28	CHR00012287-RA	正向 Forward	1 389	2	462	6.2	53.3
CnGRAS29	CHR00001229-RA	反向 Reverse	1 659	5	552	6.4	62.5
CnGRAS30	CHR00090421-RA	正向 Forward	1 326	5	441	5.8	50.0
CnGRAS31	CHR00090422-RA	正向 Forward	1 770	12	589	8.2	67.0
CnGRAS32	CHR00006827-RA	反向 Reverse	1 989	4	662	6.5	73.5
CnGRAS33	CHR00080708-RA	反向 Reverse	1 845	7	614	5.7	68.2
CnGRAS34	CHR00009185-RA	正向 Forward	1 761	2	586	7.2	66.5
CnGRAS35	CHR00014432-RA	反向 Reverse	1 284	4	427	7.3	48.9
CnGRAS36	CHR00027166-RA	正向 Forward	1 995	5	664	5.8	73.2
CnGRAS37	CHR00030490-RA	反向 Reverse	1 221	3	406	6.1	46.3
CnGRAS38	CHR00089224-RA	反向 Reverse	1 389	8	462	5.8	51.9
CnGRAS39	CHR00032024-RA	反向 Reverse	840	2	279	7.2	31.8
CnGRAS40	CHR00059102-RA	反向 Reverse	1 176	5	391	5.1	43.2
CnGRAS41	CHR00020653-RA	反向 Reverse	660	7	219	9.1	25.6
CnGRAS42	CHR00023444-RA	正向 Forward	1 461	4	486	5.6	54.6
CnGRAS43	CHR00047978-RA	正向 Forward	2 112	5	703	7.6	79.9
CnGRAS44	CHR00037746-RA	反向（reverse）	1 350	8	449	5.7	50.2
CnGRAS45	CHR00050945-RA	正向 Forward	1 464	3	487	5.3	54.8
CnGRAS46	CHR00043205-RA	反向（reverse）	1 656	6	551	5.3	62.2
CnGRAS47	CHR00020406-RA	正向 Forward	1 047	3	348	7.7	38.9
CnGRAS48	CHR00034025-RA	反向 Reverse	1 608	3	535	5.2	59.6
CnGRAS49	CHR00074287-RA	正向 Forward	1 500	2	499	5.4	55.5
CnGRAS50	CHR00022194-RA	正向 Forward	1 269	3	422	5.7	48.2
CnGRAS51	CHR00013495-RA	正向 Forward	771	4	256	5.9	28.4
CnGRAS52	CHR00043827-RA	反向 Reverse	1 221	4	406	5.9	46.8
CnGRAS53	CHR00043828-RA	反向 Reverse	2 172	5	723	5.4	82.3
CnGRAS54	CHR00082830-RA	反向 Reverse	1 779	4	592	5.7	101.7
CnGRAS55	CHR00031262-RA	正向 Forward	1 413	3	470	8.0	53.8
CnGRAS56	CHR00066643-RA	正向 Forward	2 175	7	724	5.3	82.6
CnGRAS57	CHR00036461-RA	正向 Forward	1 665	5	554	6.3	61.9
CnGRAS58	CHR00037682-RA	反向 Reverse	1 548	3	515	6.0	56.4
CnGRAS59	CHR00081984-RA	正向 Forward	963	2	320	8.6	37.1
CnGRAS60	CHR00076473-RA	反向 Reverse	1 209	2	402	5.4	44.2
CnGRAS61	CHR00077126-RA	正向 Forward	1 326	6	441	5.2	49.7
CnGRAS62	CHR00021855-RA	正向 Forward	1 356	4	451	5.9	50.9
CnGRAS63	CHR00039693-RA	反向 Reverse	1 584	4	527	5.6	58.6
CnGRAS64	CHR00022872-RA	正向 Forward	1 023	4	340	5.0	37.8
CnGRAS65	CHR00086408-RA	反向 Reverse	1 323	3	440	5.1	49.7
CnGRAS66	CHR00081508-RA	正向 Forward	1 632	4	543	6.3	61.2
CnGRAS67	CHR00087940-RA	反向 Reverse	1 878	5	625	5.4	69.6
CnGRAS68	CHR00058033-RA	反向 Reverse	1 488	3	495	7.5	54.8
CnGRAS69	CHR00087040-RA	反向 Reverse	1 032	4	343	6.0	39.3
CnGRAS70	CHR00087041-RA	反向 Reverse	1 914	10	637	5.4	71.9
CnGRAS71	CHR00087042-RA	反向 Reverse	1 446	3	481	5.9	54.8
CnGRAS72	CHR00087043-RA	反向 Reverse	2 208	4	735	4.9	83.8
CnGRAS73	CHR00087044-RA	反向 Reverse	969	8	322	8.2	36.3
CnGRAS74	CHR00087600-RA	反向 Reverse	1 371	4	456	6.2	51.3
CnGRAS75	CHR00091555-RA	反向 Reverse	1 257	4	418	5.3	46.5
CnGRAS76	CHR00065020-RA	反向 Reverse	1 581	5	526	4.8	57.4
CnGRAS77	CHR00065743-RA	正向 Forward	1 515	6	504	6.1	57.8
CnGRAS78	CHR00069367-RA	正向 Forward	1 488	6	495	5.3	54.2
CnGRAS79	CHR00093834-RA	反向 Reverse	705	3	234	4.6	26.1
CnGRAS80	CHR00074223-RA	正向 Forward	735	5	244	9.1	28.6

基因名 Gene name	基因ID Gene ID	方向 Strand	开放阅读框/bp ORF	外显子数 Number of exons	蛋白质/aa Protein	等电点 pI	分子量/kD MW
CnGRAS1	CHR00004937-RA	反向 Reverse	1 401	6	466	4.6	52.8
CnGRAS2	CHR00004939-RA	反向 Reverse	948	6	315	4.5	35.8
CnGRAS3	CHR00004941-RA	反向 Reverse	1 305	4	434	4.6	48.9
CnGRAS4	CHR00004943-RA	反向 Reverse	1 005	5	334	5.0	37.9
CnGRAS5	CHR00010605-RA	反向 Reverse	1 464	3	487	5.7	54.8
CnGRAS6	CHR00010606-RA	反向 Reverse	1 551	6	516	5.5	57.9
CnGRAS7	CHR00030831-RA	反向 Reverse	1 317	6	438	5.3	49.3
CnGRAS8	CHR00009270-RA	反向 Reverse	882	3	293	5.2	33.7
CnGRAS9	CHR00003961-RA	反向 Reverse	3 216	3	1 071	5.5	121.1
CnGRAS10	CHR00055273-RA	反向 Reverse	762	4	253	5.7	28.5
CnGRAS11	CHR00032218-RA	反向 Reverse	1 407	2	468	6.1	52.6
CnGRAS12	CHR00031862-RA	正向 Forward	624	3	207	8.9	22.7
CnGRAS13	CHR00060013-RA	正向 Forward	2 187	7	728	5.1	81.5
CnGRAS14	CHR00049603-RA	反向 Reverse	1 965	3	654	5.5	71.8
CnGRAS15	CHR00044507-RA	正向 Forward	1 587	2	528	5.9	59.0
CnGRAS16	CHR00088841-RA	正向 Forward	684	2	227	6.4	25.3
CnGRAS17	CHR00057450-RA	反向 Reverse	1 809	4	602	6.4	66.5
CnGRAS18	CHR00032070-RA	正向 Forward	1 605	4	534	5.8	61.0
CnGRAS19	CHR00001839-RA	正向 Forward	1 656	1	551	6.2	62.0
CnGRAS20	CHR00003428-RA	正向 Forward	1 560	3	519	4.9	58.8
CnGRAS21	CHR00080196-RA	反向 Reverse	1 863	4	620	5.8	69.5
CnGRAS22	CHR00056344-RA	反向 Reverse	1 509	5	502	5.2	56.5
CnGRAS23	CHR00043261-RA	反向 Reverse	1 617	6	538	5.4	61.0
CnGRAS24	CHR00007360-RA	正向 Forward	1 647	6	548	5.7	61.3
CnGRAS25	CHR00084234-RA	反向 Reverse	1 971	5	656	6.3	75.5
CnGRAS26	CHR00026458-RA	正向 Forward	1 587	7	528	5.1	59.7
CnGRAS27	CHR00012285-RA	正向 Forward	1 392	5	463	5.8	53.1
CnGRAS28	CHR00012287-RA	正向 Forward	1 389	2	462	6.2	53.3
CnGRAS29	CHR00001229-RA	反向 Reverse	1 659	5	552	6.4	62.5
CnGRAS30	CHR00090421-RA	正向 Forward	1 326	5	441	5.8	50.0
CnGRAS31	CHR00090422-RA	正向 Forward	1 770	12	589	8.2	67.0
CnGRAS32	CHR00006827-RA	反向 Reverse	1 989	4	662	6.5	73.5
CnGRAS33	CHR00080708-RA	反向 Reverse	1 845	7	614	5.7	68.2
CnGRAS34	CHR00009185-RA	正向 Forward	1 761	2	586	7.2	66.5
CnGRAS35	CHR00014432-RA	反向 Reverse	1 284	4	427	7.3	48.9
CnGRAS36	CHR00027166-RA	正向 Forward	1 995	5	664	5.8	73.2
CnGRAS37	CHR00030490-RA	反向 Reverse	1 221	3	406	6.1	46.3
CnGRAS38	CHR00089224-RA	反向 Reverse	1 389	8	462	5.8	51.9
CnGRAS39	CHR00032024-RA	反向 Reverse	840	2	279	7.2	31.8
CnGRAS40	CHR00059102-RA	反向 Reverse	1 176	5	391	5.1	43.2
CnGRAS41	CHR00020653-RA	反向 Reverse	660	7	219	9.1	25.6
CnGRAS42	CHR00023444-RA	正向 Forward	1 461	4	486	5.6	54.6
CnGRAS43	CHR00047978-RA	正向 Forward	2 112	5	703	7.6	79.9
CnGRAS44	CHR00037746-RA	反向（reverse）	1 350	8	449	5.7	50.2
CnGRAS45	CHR00050945-RA	正向 Forward	1 464	3	487	5.3	54.8
CnGRAS46	CHR00043205-RA	反向（reverse）	1 656	6	551	5.3	62.2
CnGRAS47	CHR00020406-RA	正向 Forward	1 047	3	348	7.7	38.9
CnGRAS48	CHR00034025-RA	反向 Reverse	1 608	3	535	5.2	59.6
CnGRAS49	CHR00074287-RA	正向 Forward	1 500	2	499	5.4	55.5
CnGRAS50	CHR00022194-RA	正向 Forward	1 269	3	422	5.7	48.2
CnGRAS51	CHR00013495-RA	正向 Forward	771	4	256	5.9	28.4
CnGRAS52	CHR00043827-RA	反向 Reverse	1 221	4	406	5.9	46.8
CnGRAS53	CHR00043828-RA	反向 Reverse	2 172	5	723	5.4	82.3
CnGRAS54	CHR00082830-RA	反向 Reverse	1 779	4	592	5.7	101.7
CnGRAS55	CHR00031262-RA	正向 Forward	1 413	3	470	8.0	53.8
CnGRAS56	CHR00066643-RA	正向 Forward	2 175	7	724	5.3	82.6
CnGRAS57	CHR00036461-RA	正向 Forward	1 665	5	554	6.3	61.9
CnGRAS58	CHR00037682-RA	反向 Reverse	1 548	3	515	6.0	56.4
CnGRAS59	CHR00081984-RA	正向 Forward	963	2	320	8.6	37.1
CnGRAS60	CHR00076473-RA	反向 Reverse	1 209	2	402	5.4	44.2
CnGRAS61	CHR00077126-RA	正向 Forward	1 326	6	441	5.2	49.7
CnGRAS62	CHR00021855-RA	正向 Forward	1 356	4	451	5.9	50.9
CnGRAS63	CHR00039693-RA	反向 Reverse	1 584	4	527	5.6	58.6
CnGRAS64	CHR00022872-RA	正向 Forward	1 023	4	340	5.0	37.8
CnGRAS65	CHR00086408-RA	反向 Reverse	1 323	3	440	5.1	49.7
CnGRAS66	CHR00081508-RA	正向 Forward	1 632	4	543	6.3	61.2
CnGRAS67	CHR00087940-RA	反向 Reverse	1 878	5	625	5.4	69.6
CnGRAS68	CHR00058033-RA	反向 Reverse	1 488	3	495	7.5	54.8
CnGRAS69	CHR00087040-RA	反向 Reverse	1 032	4	343	6.0	39.3
CnGRAS70	CHR00087041-RA	反向 Reverse	1 914	10	637	5.4	71.9
CnGRAS71	CHR00087042-RA	反向 Reverse	1 446	3	481	5.9	54.8
CnGRAS72	CHR00087043-RA	反向 Reverse	2 208	4	735	4.9	83.8
CnGRAS73	CHR00087044-RA	反向 Reverse	969	8	322	8.2	36.3
CnGRAS74	CHR00087600-RA	反向 Reverse	1 371	4	456	6.2	51.3
CnGRAS75	CHR00091555-RA	反向 Reverse	1 257	4	418	5.3	46.5
CnGRAS76	CHR00065020-RA	反向 Reverse	1 581	5	526	4.8	57.4
CnGRAS77	CHR00065743-RA	正向 Forward	1 515	6	504	6.1	57.8
CnGRAS78	CHR00069367-RA	正向 Forward	1 488	6	495	5.3	54.2
CnGRAS79	CHR00093834-RA	反向 Reverse	705	3	234	4.6	26.1
CnGRAS80	CHR00074223-RA	正向 Forward	735	5	244	9.1	28.6

基因对 Gene pair		非同义替换率（Ka） Non-synonymous substitution rate	同义替换率（Ks） Synonymous substitution rate	Ka/Ks	复制时间/Myr Duplication date	纯化选择 Purifying selection
CnGRAS2	CnGRAS3	0.038	0.087	0.438	2.9	Yes
CnGRAS5	CnGRAS6	0.151	0.555	0.272	18.5	Yes
CnGRAS27	CnGRAS28	0.024	0.080	0.305	2.7	Yes
CnGRAS30	CnGRAS31	0.470	2.249	0.209	75.0	Yes
CnGRAS52	CnGRAS53	0.142	0.415	0.344	13.8	Yes
CnGRAS69	CnGRAS70	0.275	0.821	0.335	27.4	Yes
CnGRAS70	CnGRAS71	0.116	0.150	0.769	5.0	Yes
CnGRAS71	CnGRAS72	0.145	0.271	0.534	9.0	Yes
CnGRAS72	CnGRAS73	0.630	2.365	0.266	78.8	Yes

基因对 Gene pair		非同义替换率（Ka） Non-synonymous substitution rate	同义替换率（Ks） Synonymous substitution rate	Ka/Ks	复制时间/Myr Duplication date	纯化选择 Purifying selection
CnGRAS2	CnGRAS3	0.038	0.087	0.438	2.9	Yes
CnGRAS5	CnGRAS6	0.151	0.555	0.272	18.5	Yes
CnGRAS27	CnGRAS28	0.024	0.080	0.305	2.7	Yes
CnGRAS30	CnGRAS31	0.470	2.249	0.209	75.0	Yes
CnGRAS52	CnGRAS53	0.142	0.415	0.344	13.8	Yes
CnGRAS69	CnGRAS70	0.275	0.821	0.335	27.4	Yes
CnGRAS70	CnGRAS71	0.116	0.150	0.769	5.0	Yes
CnGRAS71	CnGRAS72	0.145	0.271	0.534	9.0	Yes
CnGRAS72	CnGRAS73	0.630	2.365	0.266	78.8	Yes

Genome-wide Identification and Expression Analysis of the GRAS Gene Family in Response to Cold Stress in Chrysanthemum nankingense

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