Analysis of Meta-quantitative Trait Loci and Their Candidate Genes Related to Leaf Shape in Maize

doi:10.11983/CBB17082

Abstract

Abstract:

Leaf length, width, area, and angle are important components of plant architecture but also affect the efficiency of photosynthesis in maize. In this study, 620 quantitative trait loci (QTL) were used to construct an integrated map related to maize leaf shape; 22 maize QTL (mQTL) for leaf length, 22 for leaf width, 12 for leaf area and 17 for leaf angle were estimated by meta-analysis. Further bioinformatics analysis identified 44 candidate genes closely related to leaf shape within the mQTL region, with some unintegrated QTL. However, only 13 candidate genes, including NAL7-like, YABBY6-like, and GRF2, were located in the mQTL region. Most of the candidate genes, such as the cloned genes KNOTTED1, AN3/GIF1, rgd1/lbl1 and mwp1 in maize and SRL2-like, HYL1-like, and CYCB2;4-like in rice and Arabidopsis thaliana homologous genes were projected onto the interval of unintegrated QTL. The regulation mechanism of 44 candidate genes is summarized and analyzed in the development of leaf length, width and thickness, by proximal-distal, central-marginal and adaxial-abaxial. Only a few known genes revealed part of the molecular mechanism of leaf deve- lopment in maize. Further research of the mQTL/QTL and related genes will create a global view of the genetic architecture of maize leaf shape, provide useful biological information for fine mapping QTL, and identify more candidate genes to clarify the molecular mechanism of leaf morphogenesis and provide a theoretical base for ideal plant-architecture improvement of maize marker-assisted breeding.

Key words: maize (Zea mays), leaf length, leaf width, leaf area, leaf angle, meta-analysis, meta-QTL, candidate gene

Guo Shulei, Zhang Jun, Qi Jianshuang, Yue Runqing, Han Xiaohua, Yan Shufeng, Lu Caixia, Fu Xiaolei, Chen Nana, Ku Lixia, Tie Shuanggui. Analysis of Meta-quantitative Trait Loci and Their Candidate Genes Related to Leaf Shape in Maize[J]. Chinese Bulletin of Botany, 2018, 53(4): 487-501.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB17082

https://www.chinbullbotany.com/EN/Y2018/V53/I4/487

Figures/Tables 4

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Parents	Type of Pop.	Pop. size	No. of QTL for LL	No. of QTL for LW	No. of QTL for LAr	No. of QTL for LA	No./type of marker	Analysis method	Reference
B73×G79	F_2:3	214	—	—	7	—	185/RFLP	IM	Agrama et al., 1999
B73×Mo17	RIL	180	—	—	—	9	192/SSR	CIM	Mickelson et al., 2002
H21×Mo17	F2:3	120	—	—	—	7	102/SSR	CIM	于永涛等, 2006
Zi330×K36	F2:3	114	—	—	—	2	90/SSR	CIM	于永涛等, 2006
Ye478×Dan340	F2:3	397	—	—	—	6	138/SSR	CIM	路明等, 2007
Mo17×Huangzao4	RIL	239	4	2	5	—	98/SSR	CIM	郑祖平等, 2007
Ye478×Wu312	RIL	218	—	—	7	—	184/SSR	ICIM	刘建超等, 2010
Yu82×Shen137	F2:3	229	3	4	13	3	222/SSR	CIM	Ku et al., 2010, 2012a
Yu82×Yu87-1	F2:3	256	5	5	—	5	216/SSR	CIM	Ku et al., 2012b
B73/Mo17 etc.	NAM	4892	36	34	—	30	203000/SNP	GWAS	Tian et al., 2011
N6×BT-1	RIL	250	—	—	6	—	207/SSR	CIM	李贤唐等, 2011
Y105×Y106	F2	189	5	7	6	8	215/SSR	ICIM	郭莹, 2012
Y114×Y115	F2	189	1	1	2	3	204/SSR	ICIM	郭莹, 2012
Ye478×Wu312	RIL	218	14	7	9	—	184/SSR	CIM	Cai et al., 2012
Yu82×D132	F2:3	245	—	—	18	—	204/SSR	CIM	Ku et al., 2012
B73×1212	RIL	325	67	62	—	—	208/SSR	ICIM	唐登国, 2013
B73×Mo17	RIL	93	1	2	—	3	IBM2 map	CIM	Wassom, 2013
CY5×YL106	F2:3	144	—	—	—	8	212/SSR	CIM	刘正等, 2014
Z58/87-1// PH6WC/Zi330	CP	228	—	—	—	13	225/SSR	IM	张姿丽等, 2014b
T4×T19	F2:3	232	—	—	4	—	81/SSR	CIM	张姿丽等, 2014a
Yu82×Yu87-1	RIL	208	—	18	—	—	1370/SNP	CIM	Guo et al., 2015
Yu82×Shen137	RIL	197	—	9	—	—	1411/SNP	CIM	Guo et al., 2015
Zong3×Yu87-1	RIL	223	—	10	—	—	1479/SNP	CIM	Guo et al., 2015
Yu537A×Shen137	RIL	212	—	9	—	—	1371/SNP	CIM	Guo et al., 2015
B73×Mo17	DH	221	9	17	16	12	5935/bin markers	ICIM	张志腾, 2015
Xu178×K12	RIL	150	—	—	—	34	191/SSR	CIM	常立国等, 2016
M1-7×SYF	F₂	259	—	—	36	—	218/SSR	CIM	安允权等, 2016
Yu82×D132	RIL	234	5	7	4	—	1226/SNP	CIM	Wei et al., 2016

Parents	Type of Pop.	Pop. size	No. of QTL for LL	No. of QTL for LW	No. of QTL for LAr	No. of QTL for LA	No./type of marker	Analysis method	Reference
B73×G79	F_2:3	214	—	—	7	—	185/RFLP	IM	Agrama et al., 1999
B73×Mo17	RIL	180	—	—	—	9	192/SSR	CIM	Mickelson et al., 2002
H21×Mo17	F2:3	120	—	—	—	7	102/SSR	CIM	于永涛等, 2006
Zi330×K36	F2:3	114	—	—	—	2	90/SSR	CIM	于永涛等, 2006
Ye478×Dan340	F2:3	397	—	—	—	6	138/SSR	CIM	路明等, 2007
Mo17×Huangzao4	RIL	239	4	2	5	—	98/SSR	CIM	郑祖平等, 2007
Ye478×Wu312	RIL	218	—	—	7	—	184/SSR	ICIM	刘建超等, 2010
Yu82×Shen137	F2:3	229	3	4	13	3	222/SSR	CIM	Ku et al., 2010, 2012a
Yu82×Yu87-1	F2:3	256	5	5	—	5	216/SSR	CIM	Ku et al., 2012b
B73/Mo17 etc.	NAM	4892	36	34	—	30	203000/SNP	GWAS	Tian et al., 2011
N6×BT-1	RIL	250	—	—	6	—	207/SSR	CIM	李贤唐等, 2011
Y105×Y106	F2	189	5	7	6	8	215/SSR	ICIM	郭莹, 2012
Y114×Y115	F2	189	1	1	2	3	204/SSR	ICIM	郭莹, 2012
Ye478×Wu312	RIL	218	14	7	9	—	184/SSR	CIM	Cai et al., 2012
Yu82×D132	F2:3	245	—	—	18	—	204/SSR	CIM	Ku et al., 2012
B73×1212	RIL	325	67	62	—	—	208/SSR	ICIM	唐登国, 2013
B73×Mo17	RIL	93	1	2	—	3	IBM2 map	CIM	Wassom, 2013
CY5×YL106	F2:3	144	—	—	—	8	212/SSR	CIM	刘正等, 2014
Z58/87-1// PH6WC/Zi330	CP	228	—	—	—	13	225/SSR	IM	张姿丽等, 2014b
T4×T19	F2:3	232	—	—	4	—	81/SSR	CIM	张姿丽等, 2014a
Yu82×Yu87-1	RIL	208	—	18	—	—	1370/SNP	CIM	Guo et al., 2015
Yu82×Shen137	RIL	197	—	9	—	—	1411/SNP	CIM	Guo et al., 2015
Zong3×Yu87-1	RIL	223	—	10	—	—	1479/SNP	CIM	Guo et al., 2015
Yu537A×Shen137	RIL	212	—	9	—	—	1371/SNP	CIM	Guo et al., 2015
B73×Mo17	DH	221	9	17	16	12	5935/bin markers	ICIM	张志腾, 2015
Xu178×K12	RIL	150	—	—	—	34	191/SSR	CIM	常立国等, 2016
M1-7×SYF	F₂	259	—	—	36	—	218/SSR	CIM	安允权等, 2016
Yu82×D132	RIL	234	5	7	4	—	1226/SNP	CIM	Wei et al., 2016

Bin	mQTL/QTL	CI (cM)	Candidate gene	Annotation	Homologous gene	E-value	Reference
1.02	mQTLW1-1	153.8-158.3	GRMZM2G480386	NAL7-like	Os03g0162000/YUCCA7	0	Fujino et al., 2008
1.04	q12SevLW1	270.6-286.2	GRMZM2G011483	SRL2-like	Os03g19520/SRL2	0	Liu et al., 2016
1.05	mQTLW1-2	485.9-505.6	GRMZM2G141955	YABBY6-like	Os12g42610/YAB6	3E-88	Toriba et al., 2007; Zhang et al., 2009
1.05	mQTLW1-2	485.9-505.6	GRMZM2G003509	PHB-like	AT2G34710/AtHB14	0	Kim et al., 2003; Mallory et al., 2004
1.09	mQTLW1-3	820.6-845.5	GRMZM2G018414	GRF8	AT4G37740/AtGRF2	4E-37	Debernardi et al., 2014
1.10	q4LWm139	873.7-902.1	GRMZM2G017087	KNOTTED1	AT4G08150/KN1	2E-114	Ramirez et al., 2009
			GRMZM2G178261	GRF1-like	AT2G22840/AtGRF1	2E-66	Kim et al., 2003
			GRMZM2G180246	AN3/GIF1	AT5G28640/AtAN3/GIF1	1E-36	Nelissen et al., 2015
1.11	q4LLm155	941.6-1022.3	GRMZM2G135447	OSH43-like	Os03g0771500/OsH43	4E-99	Sentoku et al., 2000
2.02	q3LAr2a	67.5-79.7	GRMZM2G174784	AP2-like	AT4G36920/AP2	7E-102	Würschum et al., 2006; Mlotshwa et al., 2006
2.02	mQTLW2-1	118.3-147.8	GRMZM2G102346	NAL1-like	Os04g52479/NAL1	0	Kubo et al., 2017
2.02	mQTLW2-1	118.3-147.8	GRMZM2G041223	GRF6	AT3G13960/AtGRF5	1E-36	Horiguchi et al., 2006; Debernardi et al., 2014
2.06	q4RLAr2	355.7-374.4	GRMZM2G444808	HYL1-like	AT1G09700/HYL1	6E-56	Liu et al., 2011
2.06	q8SecLW2	370.0-381.6	GRMZM2G083972	LNG2-like	AT3G02170/LNG2	6E-57	Lee et al., 2006
2.06	q8SecLW2	370.0-381.6	GRMZM2G161382	CYCD3;3-like	AT3G50070/CYCD3;3	5E-56	Dewitte et al., 2007
2.07	q7LL2b	450.0-461.9	GRMZM2G004619	GRF4	AT4G37740/AtGRF2	5E-28	Kim et al., 2003
2.10	q12LAr2	713.1-732.4	GRMZM2G146688	ANT-like	AT4G37750/ANT	1E-131	Mizukami and Fis- cher, 2000
3.02	q4LWm309	69.6-90.3	GRMZM2G143235	ROT3-like	AT4G36380/ROT3	1E-176	Kim et al., 1998
3.06	mQTLW3-2	368.5-390.3	GRMZM2G118250	AS2-like	AT1G65620/AS2	1E-66	Iwakawa et al., 2007
3.08	q4LWm410	613.6-653.7	GRMZM2G437460	ARF3-like	AT2G33860/ARF3/ETT	1E-169	Kelley et al., 2012
4.04	q13NLW4	220.5-230.6	GRMZM2G402653	OSH1-like	Os03g0727000/OsH1	1E-75	Matsuoka et al., 1993
4.06	mQTLW4	373.7-399.4	GRMZM2G124566	GRF9-like	AT2G36400/AtGRF3	1E-36	Kim et al., 2003
4.08	q7LL4	429.5-451.0	GRMZM2G075117	CYCD3;1-like	AT4G34160/CYCD3;1	4E-47	Dewitte et al., 2007
4.08	q7LL4	429.5-451.0	GRMZM2G105335	GRF3	AT3G13960/AtGRF5	8E-49	Horiguchi et al., 2006; Debernardi et al., 2014
5.03	q4LWm602	268.8-295.0	GRMZM2G361518	AGO10-like	AT5G43810/AGO10/ZLL	0	Zhu et al., 2011; Roodbarkelari et al., 2015
5.03	q4LLm605	280.1-296.1	GRMZM2G171349	COW1-like	AT4G34580/COW1	3E-66	Woo et al., 2007
5.06	q4LLm661	500.7-521.1	GRMZM2G034876	GRF1	AT3G13960/AtGRF5	1E-47	Horiguchi et al., 2006; Debernardi et al., 2014
5.07	mQTLW5-3	556.7-578.5	GRMZM5G893117	GRF9	AT3G13960/AtGRF5	1E-27	Horiguchi et al., 2006; Debernardi et al., 2014
6.01	q8FirLW6-1	82.3-93.9	GRMZM2G122537	PRS1-like	AT2G28610/PRS1	6E-29	Matsumoto and Ok- ada, 2001; Nakata et al., 2012
6.01	q8FirLW6-1	82.3-93.9	GRMZM2G020187	rgd1/lbl1	AT5G23570/SGS3	1E-157	Dotto et al., 2014
	mQTL/QTL	CI (cM)	Candidate gene	Annotation	Homologous gene	E-value	Reference
6.01	mQTLAr6	92.8-108.9	GRMZM2G098594	GRF14	AT3G13960/AtGRF5	1E-36	Horiguchi et al., 2006; Debernardi et al., 2014
6.02	q7PLL6	123.0-144.8	GRMZM2G073671	CYCB2;3-like	AT1G20610/CYCB2;3	1E-144	Eloy et al., 2011
6.02	q7PLL6	123.0-144.8	GRMZM2G157820	CLF-like	AT2G23380/CLF	0	Menges et al., 2005; Schatlowski et al., 2010
6.04	q4LWm706	158.2-205.1	GRMZM5G850129	GRF7	AT3G13960/AtGRF5	4E-41	Horiguchi et al., 2006; Debernardi et al., 2014
7.00	q4LWm762	8.0-93.0	GRMZM2G028041	OSH15-like	Os07g0129700/OsH15	1.E-168	Nagasaki et al., 2001
7.00	q4LWm762	8.0-93.0	GRMZM2G019200	DRL1-like	Os11g0312782/DRL1	0	Jun et al., 2015
7.02	q12EigLW7	200.7-217.9	GRMZM2G107377	CYCD3;2-like	AT5G67260/CYCD3;2	8E-49	Dewitte et al., 2007
7.02	q12FirLW7	229.3-246.3	GRMZM2G082264	mwp1	Os09g23200/SLL1/Kan1	2E-170	Candela et al., 2008
7.03	q3LW7	380.6-498.2	GRMZM2G096709	GRF10	AT4G37740/AtGRF2	4E-29	Kim et al., 2003; Deb- ernardi et al., 2014
8.08	q3LW8	599.1-603.8	GRMZM5G874163	ARF4-like	AT5G60450/ARF4	7E-120	Pekker et al., 2005; Hunter et al., 2006
9.03	mQTLW9	206.1-230.6	GRMZM2G119359	GRF12	AT2G06200/AtGRF6	1E-30	Kim et al., 2003; Liang et al., 2014
9.03	mQTLW9	206.1-230.6	GRMZM5G870176	NRL-like	Os12g36890/CSLD4	0	Hu et al., 2010
10.04	mQTLW10	295.6-327.3	GRMZM2G078641	GRF2	GRAT3G13960/AtGRF7	3E-156	Horiguchi et al., 2006; Debernardi et al., 2014
10.06	q1HNLAr10	367.0-383.9	GRMZM2G061287	CYCB2;4-like	AT1G76310/CYCB2;4	9E-148	Menges et al., 2005; Eloy et al., 2011

Bin	mQTL/QTL	CI (cM)	Candidate gene	Annotation	Homologous gene	E-value	Reference
1.02	mQTLW1-1	153.8-158.3	GRMZM2G480386	NAL7-like	Os03g0162000/YUCCA7	0	Fujino et al., 2008
1.04	q12SevLW1	270.6-286.2	GRMZM2G011483	SRL2-like	Os03g19520/SRL2	0	Liu et al., 2016
1.05	mQTLW1-2	485.9-505.6	GRMZM2G141955	YABBY6-like	Os12g42610/YAB6	3E-88	Toriba et al., 2007; Zhang et al., 2009
1.05	mQTLW1-2	485.9-505.6	GRMZM2G003509	PHB-like	AT2G34710/AtHB14	0	Kim et al., 2003; Mallory et al., 2004
1.09	mQTLW1-3	820.6-845.5	GRMZM2G018414	GRF8	AT4G37740/AtGRF2	4E-37	Debernardi et al., 2014
1.10	q4LWm139	873.7-902.1	GRMZM2G017087	KNOTTED1	AT4G08150/KN1	2E-114	Ramirez et al., 2009
			GRMZM2G178261	GRF1-like	AT2G22840/AtGRF1	2E-66	Kim et al., 2003
			GRMZM2G180246	AN3/GIF1	AT5G28640/AtAN3/GIF1	1E-36	Nelissen et al., 2015
1.11	q4LLm155	941.6-1022.3	GRMZM2G135447	OSH43-like	Os03g0771500/OsH43	4E-99	Sentoku et al., 2000
2.02	q3LAr2a	67.5-79.7	GRMZM2G174784	AP2-like	AT4G36920/AP2	7E-102	Würschum et al., 2006; Mlotshwa et al., 2006
2.02	mQTLW2-1	118.3-147.8	GRMZM2G102346	NAL1-like	Os04g52479/NAL1	0	Kubo et al., 2017
2.02	mQTLW2-1	118.3-147.8	GRMZM2G041223	GRF6	AT3G13960/AtGRF5	1E-36	Horiguchi et al., 2006; Debernardi et al., 2014
2.06	q4RLAr2	355.7-374.4	GRMZM2G444808	HYL1-like	AT1G09700/HYL1	6E-56	Liu et al., 2011
2.06	q8SecLW2	370.0-381.6	GRMZM2G083972	LNG2-like	AT3G02170/LNG2	6E-57	Lee et al., 2006
2.06	q8SecLW2	370.0-381.6	GRMZM2G161382	CYCD3;3-like	AT3G50070/CYCD3;3	5E-56	Dewitte et al., 2007
2.07	q7LL2b	450.0-461.9	GRMZM2G004619	GRF4	AT4G37740/AtGRF2	5E-28	Kim et al., 2003
2.10	q12LAr2	713.1-732.4	GRMZM2G146688	ANT-like	AT4G37750/ANT	1E-131	Mizukami and Fis- cher, 2000
3.02	q4LWm309	69.6-90.3	GRMZM2G143235	ROT3-like	AT4G36380/ROT3	1E-176	Kim et al., 1998
3.06	mQTLW3-2	368.5-390.3	GRMZM2G118250	AS2-like	AT1G65620/AS2	1E-66	Iwakawa et al., 2007
3.08	q4LWm410	613.6-653.7	GRMZM2G437460	ARF3-like	AT2G33860/ARF3/ETT	1E-169	Kelley et al., 2012
4.04	q13NLW4	220.5-230.6	GRMZM2G402653	OSH1-like	Os03g0727000/OsH1	1E-75	Matsuoka et al., 1993
4.06	mQTLW4	373.7-399.4	GRMZM2G124566	GRF9-like	AT2G36400/AtGRF3	1E-36	Kim et al., 2003
4.08	q7LL4	429.5-451.0	GRMZM2G075117	CYCD3;1-like	AT4G34160/CYCD3;1	4E-47	Dewitte et al., 2007
4.08	q7LL4	429.5-451.0	GRMZM2G105335	GRF3	AT3G13960/AtGRF5	8E-49	Horiguchi et al., 2006; Debernardi et al., 2014
5.03	q4LWm602	268.8-295.0	GRMZM2G361518	AGO10-like	AT5G43810/AGO10/ZLL	0	Zhu et al., 2011; Roodbarkelari et al., 2015
5.03	q4LLm605	280.1-296.1	GRMZM2G171349	COW1-like	AT4G34580/COW1	3E-66	Woo et al., 2007
5.06	q4LLm661	500.7-521.1	GRMZM2G034876	GRF1	AT3G13960/AtGRF5	1E-47	Horiguchi et al., 2006; Debernardi et al., 2014
5.07	mQTLW5-3	556.7-578.5	GRMZM5G893117	GRF9	AT3G13960/AtGRF5	1E-27	Horiguchi et al., 2006; Debernardi et al., 2014
6.01	q8FirLW6-1	82.3-93.9	GRMZM2G122537	PRS1-like	AT2G28610/PRS1	6E-29	Matsumoto and Ok- ada, 2001; Nakata et al., 2012
6.01	q8FirLW6-1	82.3-93.9	GRMZM2G020187	rgd1/lbl1	AT5G23570/SGS3	1E-157	Dotto et al., 2014
	mQTL/QTL	CI (cM)	Candidate gene	Annotation	Homologous gene	E-value	Reference
6.01	mQTLAr6	92.8-108.9	GRMZM2G098594	GRF14	AT3G13960/AtGRF5	1E-36	Horiguchi et al., 2006; Debernardi et al., 2014
6.02	q7PLL6	123.0-144.8	GRMZM2G073671	CYCB2;3-like	AT1G20610/CYCB2;3	1E-144	Eloy et al., 2011
6.02	q7PLL6	123.0-144.8	GRMZM2G157820	CLF-like	AT2G23380/CLF	0	Menges et al., 2005; Schatlowski et al., 2010
6.04	q4LWm706	158.2-205.1	GRMZM5G850129	GRF7	AT3G13960/AtGRF5	4E-41	Horiguchi et al., 2006; Debernardi et al., 2014
7.00	q4LWm762	8.0-93.0	GRMZM2G028041	OSH15-like	Os07g0129700/OsH15	1.E-168	Nagasaki et al., 2001
7.00	q4LWm762	8.0-93.0	GRMZM2G019200	DRL1-like	Os11g0312782/DRL1	0	Jun et al., 2015
7.02	q12EigLW7	200.7-217.9	GRMZM2G107377	CYCD3;2-like	AT5G67260/CYCD3;2	8E-49	Dewitte et al., 2007
7.02	q12FirLW7	229.3-246.3	GRMZM2G082264	mwp1	Os09g23200/SLL1/Kan1	2E-170	Candela et al., 2008
7.03	q3LW7	380.6-498.2	GRMZM2G096709	GRF10	AT4G37740/AtGRF2	4E-29	Kim et al., 2003; Deb- ernardi et al., 2014
8.08	q3LW8	599.1-603.8	GRMZM5G874163	ARF4-like	AT5G60450/ARF4	7E-120	Pekker et al., 2005; Hunter et al., 2006
9.03	mQTLW9	206.1-230.6	GRMZM2G119359	GRF12	AT2G06200/AtGRF6	1E-30	Kim et al., 2003; Liang et al., 2014
9.03	mQTLW9	206.1-230.6	GRMZM5G870176	NRL-like	Os12g36890/CSLD4	0	Hu et al., 2010
10.04	mQTLW10	295.6-327.3	GRMZM2G078641	GRF2	GRAT3G13960/AtGRF7	3E-156	Horiguchi et al., 2006; Debernardi et al., 2014
10.06	q1HNLAr10	367.0-383.9	GRMZM2G061287	CYCB2;4-like	AT1G76310/CYCB2;4	9E-148	Menges et al., 2005; Eloy et al., 2011

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