Gene duplications and functional divergence analyses of the SPL gene family

doi:10.3969/j.issn.1000-2006.201912052

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2020, Vol. 44 ›› Issue (5): 55-66.doi: 10.3969/j.issn.1000-2006.201912052

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Gene duplications and functional divergence analyses of the SPL gene family

CHEN Wenwen(), WU Huaitong, CHEN Yingnan^*()

Key Laboratory of Forest Genetics and Biotechnology of Ministry of Education, Co-Innovation Center for the Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing 210037, China

Received:2019-12-27 Revised:2020-07-08 Online:2020-10-30 Published:2020-10-30
Contact: CHEN Yingnan E-mail:chenww@njfu.edu.cn;chenyingnan@njfu.edu.cn

Abstract

Abstract:

【Objective】Duplication and subsequent divergence of genes play important roles in driving the evolution of genomes and species. The SQUAMOSA promoter-binding-like (SPL) genes be long to a family of plant-specific transcription factors that regulate numerous fundamental aspects of plant growth and development as well as stress response. The SPL gene family provides an excellent system to analyze the evolutionary fate and consequences of duplicated genes. In this study, gene duplication and the functional divergence of the SPL gene family were analyzed in four model plants, including Vitis vinifera, Carica papaya, Populus trichocarpa and Arabidopsis thaliana. 【Method】The SPL genes of V. vinifera, C. papaya, P. trichocarpa and A. thaliana were identified by using the conserved SQUAMOSA-PROMOTER BINDING PROTEIN domain as the query, and a phylogenetic tree was constructed with the maximum likelihood method. Based on the genome collinearity within and between species, the SPL gene duplication patterns and differential retention were identified in the four plants. The K_a/K_s values were calculated for each retained SPL paralog and ortholog, and functional divergence of these genes was analyzed. 【Result】A total of 73 SPL genes were identified in the four investigated plants, and 42 of them were miR156 target genes. The phylogenetic analysis revealed that the 73 SPL genes were classified into nine major clades, with the miR156 targets being clustered in six major clades. The SPL genes in Clade I encoded two zinc finger motifs, namely C4 and C₂HC, while genes in the remaining clades encoded C3H and C₂HC. Large-scale duplication events (segmental or whole-genome duplication) have played important roles in SPL gene expansion. Based on whole-genome duplications in each species, there were theoretically 360 loci duplicated from 15 ancestral loci; however, 83.6% of them were lost or evolved into non-SPL genes. Among the retained SPL genes, 17 paralogous and 27 orthologous pairs were identified, and the K_a/K_s values of all paralogous and orthologous pairs were lower than 1. 【Conclusion】The SPL genes originating from the ancestor have differentially been retained and expanded in the genomes of the four model plants. Orthologous or paralogous SPL pairs are under strong purifying selection and show conserved structure and function, leading to strong functional conservation. Additionally, an emerging pattern of divergence, including expression bias, subfunctionalization, and neofunctionalization, was revealed among the paralogous SPL pairs. Our findings provide phylogenetic information for studying gene function and identifying species-specific genes.

Key words: SPL gene family, miR156, whole-genome duplication, tandem duplication, functional divergence

CLC Number:

S718
Q78

CHEN Wenwen, WU Huaitong, CHEN Yingnan. Gene duplications and functional divergence analyses of the SPL gene family[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2020, 44(5): 55-66.

Figures/Tables 10

Table 1

The SPL family members in A. thaliana, C. papaya, P. trichocarpa and V. vinifera"

基因名称 gene name		基因号 gene ID	染色体编号 chromosome No.		染色体上位置/bp chromosome location		蛋白质长度/aa protein		分子量/ku molecular weight		等电点 pI
AtSPL1		AT2G47070	At2		19336653—19340869		881		98.46		5.55
AtSPL2		AT5G43270	At5		17360287—17363678		450		46.86		8.85
AtSPL3		AT2G33810	At2		14305001—14306072		131		15.30		8.23
AtSPL4		AT1G53160	At1		19806263—19807705		174		20.12		9.69
AtSPL5		AT3G15270	At3		5140365—5142323		181		20.99		9.82
AtSPL6		AT1G69170	At1		26005068—26007368		405		45.95		7.60
AtSPL7		AT5G18830	At5		6275990—6280567		801		89.62		6.39
AtSPL8		AT1G02065	At1		365209—367443		333		36.83		9.01
AtSPL9		AT2G42200	At2		17587169—17589671		375		40.85		8.40
AtSPL10		AT1G27370	At1		9505115—9508542		396		44.16		7.94
AtSPL11		AT1G27360	At1		9500894—9504023		393		43.86		8.35
AtSPL12		AT3G60030	At3		22165580—22169984		927		104.14		5.85
AtSPL13a		AT5G50570	At5		20582083—20584547		359		39.11		8.03
AtSPL13b		AT5G50670	At5		20615565—20617538		359		39.11		8.03
AtSPL14		AT1G20980	At1		7324471—7329441		1 035		114.81		8.71
AtSPL15		AT3G57920	At3		21444243—21446035		354		39.67		9.11
基因名称 gene name	基因号 gene ID			染色体编号 chromosome No.		染色体上位置/bp chromosome location		蛋白质长度/aa protein		分子量/ku molecular weight	等电点 pI
AtSPL16	AT1G76580			At1		28734207—28738967		1020		113.39	8.87
CpSPL1	evm.TU.supercontig_1141.2			CpC1141		11473—13538		207		23.26	9.15
CpSPL2	evm.TU.supercontig_146.32			CpC146		148809—154539		1 008		112.30	7.32
CpSPL3	evm.TU.supercontig_149.10			CpC149		245685—247462		320		35.63	8.79
CpSPL4	evm.TU.supercontig_149.2			CpC149		88003—88868		202		22.39	9.20
CpSPL5	evm.TU.supercontig_27.40			CpC27		414724—417409		145		16.45	6.53
CpSPL6	evm.TU.supercontig_2783.1			CpC2783		2430—5568		282		31.35	9.08
CpSPL7	evm.TU.supercontig_36.105			CpC36		809951—813921		950		105.69	7.04
CpSPL8	evm.TU.supercontig_43.66			CpC43		758193—759844		388		42.58	8.98
CpSPL9	evm.TU.supercontig_6.327			CpC6		2370660—2371893		192		22.51	8.64
CpSPL10	evm.TU.supercontig_80.88			CpC80		637827—638584		187		20.88	9.17
PtSPL1	Potri.010G154000			Pt10		16159112—16166168		1 030		114.79	8.13
PtSPL2	Potri.002G002400			Pt2		156428—162756		1 073		119.09	8.53
PtSPL3	Potri.010G026200			Pt10		3686616—3693619		782		87.60	6.49
PtSPL4	Potri.008G197000			Pt8		13768389—13775909		793		88.91	6.43
PtSPL5	Potri.008G098600			Pt8		6182044—6189608		1 035		115.39	7.30
PtSPL6	Potri.014G114300			Pt14		8925158—8931521		1 004		111.26	6.13
PtSPL7	Potri.002G188700			Pt2		14848271—14855347		974		108.03	5.85
PtSPL8	Potri.002G142400			Pt2		10555550—10558359		398		43.78	8.53
PtSPL9	Potri.005G258700			Pt5		25772985—25779306		1 072		118.59	8.14
PtSPL11	Potri.003G172600			Pt3		18214192—18218896		391		43.15	9.48
PtSPL12	Potri.008G097900			Pt8		6119874—6124808		510		55.87	7.25
PtSPL13	Potri.010G154300			Pt10		16207800—16212101		498		54.54	7.87
PtSPL14	Potri.015G098900			Pt15		11818906—11822200		381		41.81	8.68
PtSPL15	Potri.012G100700			Pt12		12588839—12592476		330		36.48	8.68
PtSPL16	Potri.011G055900			Pt11		4906262—4910399		144		16.19	6.53
PtSPL17	Potri.016G048500			Pt16		3078331—3082574		382		41.03	9.03
PtSPL18	Potri.001G058600			Pt1		4478280—4482221		376		41.28	9.30
PtSPL19	Potri.001G055900			Pt1		4224329—4230450		446		49.01	8.67
PtSPL20	Potri.001G398200			Pt1		41919369—41921507		244		27.43	9.07
PtSPL21	Potri.002G142200			Pt2		10545894—10548075		325		36.13	9.11
PtSPL22	Potri.003G169400			Pt3		17943899—17947848		313		34.23	9.23
PtSPL23	Potri.004G046700			Pt4		3572260—3574124		148		16.47	7.60
PtSPL24	Potri.007G138800			Pt7		15022763—15026218		202		22.71	9.49
PtSPL25	Potri.011G116800			Pt11		14192309—14194697		242		27.24	8.93
PtSPL26	Potri.014G057700			Pt14		4451810—4454523		328		36.45	8.85
PtSPL27	Potri.014G057800			Pt14		4465308—4468876		408		45.20	6.81
PtSPL28	Potri.015G060400			Pt15		8281357—8286119		561		61.61	8.39
PtSPL29	Potri.018G149900			Pt18		16797089—16803132		472		51.72	8.58
VvSBP1	GSVIVT01012247001			Vv1		230334—235218		498		55.06	8.42
VvSBP2	GSVIVT01010496001			Vv1		21064305—21071687		418		45.94	8.96
VvSBP3	GSVIVT01010522001			Vv1		21412776—21417820		421		46.18	8.48
VvSBP4	GSVIVT01003836001			Vv4		20536349—20537931		207		24.34	5.98
VvSBP5	GSVIVT01017678001			Vv5		2565343—2574143		980		109.55	7.98
VvSBP6	GSVIVT01017835001			Vv5		3885149—3896071		692		77.30	8.08
VvSBP7	GSVIVT01028208001			Vv7		4628142—4637596		860		96.05	6.03
VvSBP8	GSVIVT01033519001			Vv8		20046489—20051103		349		37.83	9.06
VvSBP9	GSVIVT01021087001			Vv10		1346397—1348752		140		15.72	8.23
VvSBP10	GSVIVT01032239001			Vv11		13588595—13606856		326		36.70	9.47
VvSBP11	GSVIVT01020578001			Vv12		4108297—4110237		169		19.19	9.17
VvSBP12	GSVIVT01033064001			Vv14		25486818—25489754		378		42.11	8.74
VvSBP13	GSVIVT01018205001			Vv15		13245041—13249262		404		44.85	7.04
VvSBP14	GSVIVT01018204001			Vv15		13256865—13259160		388		43.51	8.58
VvSBP15	GSVIVT01008556001			Vv17		904847—907405		377		41.17	7.24
VvSBP16	XM_002265167.1			Vv17		5505520—5513472		557		61.08	6.72
VvSBP17	GSVIVT01013452001			Vv18		347645—353985		921		102.27	8.82
VvSBP18	GSVIVT01014302001			Vv19		2484297—2485658		204		22.68	8.57

Table 1

Fig.1

Fig.2

Fig.3

Fig.4

Fig.5

Table 2

Paralogous and orthologous SPL gene pairs and their Ka/Ks values"

相似性类型 type	基因对gene pair	K_a	K_s	K_a/K_s	相似性类型 type	基因对gene pair	K_a	K_s	K_a/K_s
旁系同源 paralogous	AtSPL4-AtSPL5	0.153 8	0.570 7	0.269 5	直系同源 orthologous	AtSPL5-CpSPL10	0.307 6	1.771 8	0.173 6
	AtSPL9-AtSPL15	0.269 1	0.880 4	0.305 6		AtSPL5-PtSPL20	0.355 0	1.512 0	0.234 8
	AtSPL14-AtSPL16	0.151 3	0.663 6	0.228 1		AtSPL6-PtSPL12	0.561 6	1.878 3	0.299 0
	PtSPL1-PtSPL5	0.065 6	0.225 7	0.290 8		AtSPL6-VvSBP1	0.533 5	1.465 4	0.364 1
	PtSPL1-PtSPL6	0.280 3	1.077 4	0.260 2		AtSPL7-PtSPL4	0.382 2	2.101 8	0.181 9
	PtSPL5-PtSPL6	0.281 5	1.265 9	0.222 4		AtSPL7-VvSBP6	0.396 9	1.963 5	0.202 2
	PtSPL6-PtSPL7	0.051 5	0.243 5	0.211 6		AtSPL9-PtSPL17	0.451 3	3.362 8	0.134 2
	PtSPL2-PtSPL9	0.064 6	0.264 8	0.244 1		AtSPL13b-PtSPL14	0.449 8	2.521 1	0.178 4
	PtSPL3-PtSPL4	0.083 1	0.222 3	0.373 9		AtSPL13b-VvSBP15	0.456 1	2.284 4	0.199 6
	PtSPL8-PtSPL27	0.071 5	0.284 9	0.250 9		AtSPL14-PtSPL9	0.285 1	1.545 8	0.184 4
	PtSPL11-PtSPL19	0.118 5	0.248 6	0.476 7		AtSPL14-VvSBP17	0.264 2	2.262 2	0.116 8
	PtSPL12-PtSPL13	0.100 3	0.236 6	0.424 1		PtSPL4-VvSBP6	0.251 4	1.305 1	0.192 6
	PtSPL14-PtSPL15	0.112 2	0.300 9	0.373 0		PtSPL5-VvSBP5	0.196 3	1.074 1	0.182 7
	PtSPL16-PtSPL23	0.114 3	0.258 1	0.442 9		PtSPL7-VvSBP7	0.147 3	0.909 5	0.161 9
	PtSPL18-PtSPL22	0.061 6	0.178 4	0.345 2		PtSPL9-VvSBP17	0.142 4	0.795 0	0.179 1
	PtSPL20-PtSPL25	0.078 3	0.342 8	0.228 4		PtSPL12-VvSBP1	0.325 9	0.966 0	0.337 4
	PtSPL21-PtSPL26	0.074 9	0.315 1	0.237 6		PtSPL17-VvSBP8	0.186 6	0.888 4	0.210 0
直系同源 orthologous	AtSPL1-PtSPL7	0.235 8	1.487 9	0.158 5		PtSPL18-VvSBP3	0.249 5	1.041 9	0.239 4
	AtSPL1-VvSBP7	0.246 3	1.285 5	0.191 6		PtSPL19-VvSBP2	0.301 7	0.618 0	0.488 2
	AtSPL3-PtSPL23	0.295 2	3.819 8	0.077 3		PtSPL20-CpSPL10	0.235 2	1.414 5	0.166 3
	AtSPL3-VvSBP9	0.307 8	0	-		PtSPL24-VvSBP11	0.172 7	1.230 7	0.140 3
	AtSPL4-VvSBP11	0.365 8	3.008 3	0.121 6		CpSPL10-VvSBP18	0.296 0	1.978 3	0.149 6

Table 2

Fig.6

Table 3

Table 4

Summary of SPL gene functions and GO annotations"

项目 item	基因名称 gene name	注释anmotation
功能 function	AtSPL1	生殖期花序的耐热性^[17]
	AtSPL2	植物营养生长时相转变;营养生长向生殖生长转变;花器官发育;植物生育力;负调控植株耐热性^[9,48,49]
	AtSPL3	成花诱导;过表达促进开花^[6,9,50,51]
	AtSPL4	成花诱导^[6,9]
	AtSPL5	成花诱导^[6,9]
	AtSPL6	正调控部分防御基因,提高抗病性^[16]
	AtSPL7	铜稳态调控^[44,45]
	AtSPL8	花粉囊发育;赤霉素生物合成和信号转导;植物生育力^{[10,14,52,53]}
	AtSPL9	植物营养生长时相转变;营养生长向生殖生长转变;毛状体分布;负调控叶片生长速率;负调控花色素苷合成;调节活性氧的累积和免疫反应;负调控植株耐热性^{[5,9,15,49,54-58]}
	AtSPL10	叶片形态;生殖期芽的成熟;早期胚胎发生过程中的细胞分化;抑制侧根生长;根分生组织活性和根衍生的新芽再生^[4,9,59-61]
	AtSPL11	早期胚胎发生过程中的细胞分化;叶片形态;生殖期芽的成熟;负调控植株耐热性^[4,9,49,59]
	AtSPL12	生殖期花序的耐热性^[17]
	AtSPL13a/b	植物营养生长时相转变;营养生长向生殖生长转变;调控发芽后子叶到营养叶阶段的过渡^[9,62]
	AtSPL14	对真菌毒素伏马菌素B1敏感;延缓植物幼年到成年阶段的过渡^[63]
	AtSPL15	植物营养生长时相转变;营养生长向生殖生长转变;成花诱导;负调控叶片生长速率^[5,9,47,58]
	CpSPL5	调节果实软化和类胡萝卜累积^[64]
	PtSPL3/4	基因表达量不受Cu离子浓度影响,可能参与杨树铜稳态调控^[46]
	VvSBP5	响应葡萄白粉病^[65]
	VvSBP11	成花转变,叶片发育^[42]
	VvSBP16	提高植株的耐旱性和耐盐性^[66]
GO注释 GO annotation	AtSPL16	细胞膜成分(GO:0005886);细胞核成分(GO:0005634);DNA结合(GO:0003677);金属离子结合(GO:0046872);转录调控(GO:0044212;GO:0003700;GO:0006355)
	CpSPL1	细胞核成分(GO:0005634);DNA结合(GO:0003677)
	CpSPL2	细胞大分子代谢过程(GO:0044260);ATP结合(GO:0005524);蛋白质酪氨酸激酶活性(GO:0004713);DNA结合(GO:0003677);蛋白质磷酸化(GO:0006468)细胞核成分(GO:0005634)
	CpSPL3/4/6	细胞核成分(GO:0005634);DNA结合(GO:0003677)
	CpSPL7	解旋酶活性(GO:0008026);核酸结合(GO:0003676);蛋白激酶活性(GO:0004672);DNA结合(GO:0003677)ATP结合(GO:0005524);蛋白质磷酸化(GO:0006468);细胞核成分(GO:0005634)
	CpSPL8-10	细胞核成分(GO:0005634);DNA结合(GO:0003677)
	PtSPL1/2 PtSPL5-29	细胞核成分(GO:0005634);DNA结合(GO:0003677)
	VvSBP1	细胞核成分(GO:0005634);转录调控(GO:0003700; GO:0006355)
	VvSBP6	铜离子稳态(GO:0055070);根毛细胞分化(GO:0048765);毛状体细胞形态发生(GO:0010090);细胞核成分(GO:0005634)分生组织从营养到生殖的相变(GO:0010228);转录调控(GO:0006355; GO:0003700)
	VvSBP7	调节蛋白质定位(GO:0032880);细胞核成分(GO:0005634);过氧化氢分解过程(GO:0042744);转录调控(GO:0003700;GO:0006355)
	VvSBP8	促进分生组织从营养到生殖的相变(GO:0010228);DNA转录因子活性(GO:0003700);细胞核成分(GO:0005634);叶片发育(GO:0048366;GO:2000025);花药发育(GO:0048653)
	VvSBP9	转录调控(GO:0003700; GO:0006355);细胞核成分(GO:0005634);调控营养相变(GO:0010321)
	VvSBP10	花药发育(GO:0048653);从营养期到生殖期过渡时间的调节(GO:0048510);细胞核成分(GO:0005634);转录调控(GO:0003700;GO:0006355)
	VvSBP12	花药发育(GO:0048653);转录调控(GO:0003700;GO:0006355);细胞核成分(GO:0005634)
	VvSBP14	小孢子发生(GO:0009556);大孢子发生(GO:0009554);花药发育(GO:0048653);DNA结合(GO:0003677);细胞核成分(GO:0005634)
	VvSBP15	花药发育(GO:0048653);DNA结合(GO:0003677);细胞核成分(GO:0005634)
	VvSBP17	对细菌的防御反应(GO:0042742);转录调控(GO:0045893; GO:0003700);细胞核成分(GO:0005634)
	VvSBP2-4 VvSBP13/18	未检索到GO注释

Table 4

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扩张方式 expansion method	拟南芥 A. thaliana	毛果杨 P. trichocarpa	番木瓜 C. papaya	葡萄 V. vinifera
S/WGD	12	27	6	14
串联复制 tandem duplication	2 (AtSPL10/13a)	0	0	0
其他 other	3 (AtSPL2/8/12)	1 (PtSPL29)	4 (CpSPL1/3/4/6)	4 (VvSBP4/10/14/16)
总数 total	17	28	10	18

Gene duplications and functional divergence analyses of the SPL gene family

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