SSR loci associated with population adaptation in Eucalyptus cloeziana

doi:10.3969/j.issn.1000-2006.201811018

JOURNAL OF NANJING FORESTRY UNIVERSITY ›› 2019, Vol. 43 ›› Issue (5): 59-66.doi: 10.3969/j.issn.1000-2006.201811018

SSR loci associated with population adaptation in Eucalyptus cloeziana

WANG Li¹(), LI Changrong²(), LI Fagen¹, ZHOU Changpin¹, WENG Qijie¹, LÜ Jiabin¹, CHEN Jianbo², CHEN Jiancheng³, GAN Siming¹^,²^,^*()

1. Key Laboratory of State Forestry Administration on Tropical Forestry Research, Research Institute of Tropical Forestry, Chinese Academy of Forestry, Guangzhou 510520, China
2. Guangxi Key Laboratory of Superior Timber Trees Resource Cultivation & Key Laboratory of Central South Fast-growing Timber Cultivation of Forestry Ministry of China, Guangxi Forestry Research Institute, Nanning 530002, China
3. Yulin Forestry Research Institute, Rongxian 537501, China

Received:2018-11-09 Revised:2018-12-19 Online:2019-10-08 Published:2019-10-08
Contact: GAN Siming E-mail:wangli3hao@126.com;andyharry@126.com;siminggan@caf.ac.cn

Abstract

Abstract:

【Objective】 Genomic loci that are significantly associated with population adaptation were detected inEucalyptus cloeziana F. Muell. populations to obtain useful molecular information for germplasm conservation and utilization. 【Method】 Seven northern and southern populations of E. cloeziana were analyzed using 84 simple sequence repeats (SSR) markers [29 genomic SSRs and 55 expressed sequence tag (EST) derived SSRs]. Isolation by distance (IBD) among populations was determined using Mantel test. Outlier loci ofF-statistics of between-population differentiation (F_st) and their significant allelic associations with habitat climatic variables were investigated for all the SSR loci, with further functional annotation of the significantly associated loci against the NCBI non-redundant protein database. 【Result】 IBD was revealed between the northern and southern populations of E.cloeziana, and the clustering analysis based on 19 climatic variables also resulted in division of the northern and southern populations into independent groups, suggesting the climatic effect on driving the population divergence. A total of 39 F_st outliers (46.4%) were identified as selective loci. Specifically, the software LOSITAN detected 12 positive and 17 balancing selection loci. Six alleles from five outlier loci were identified with spatial analysis methods, each associated significantly with one or more climatic factors (P < 0.001) and showed dramatic difference in allelic frequency between the northern and southern populations. Among the six significant alleles, Embra6-118 bp was associated with the minimum temperature of the coldest month ( T_mcm), with the locus Embra6 functionally annotated as basic helix-loop-helix (bHLH) transcript factor bHLH155. The allele Embra20-121 bp was associated with the precipitation of the warmest quarter (P_wq), with Embra20 functionally annotated as sucrose transporters. EUCeSSR676-168 bp was associated with T_mcm, P_wq, the mean annual temperature (T_ma) and the minimum temperature of the warmest month (T_mwm), with the locus functionally annotated as photosystem II stability/assembly factor HCF136. However, the two other significant markers EUCeSSR298 and EUCeSSR1009 were of unknown function. 【Conclusion】 The divergence between the northern and southern populations of E. cloeziana was strongly related with historical climate, and there might be glacial refugia in the northern and southern zones during the Quaternary. The marked difference in the frequency of climate-associated SSR alleles between the northern and southern populations provides molecular evidence for positive selection oriented climatic adaptation in E. cloeziana.

Key words: Eucalyptus cloeziana, SSR marker, climatic factor, positive selection, population adaptation, isolation by distance (IBD)

CLC Number:

S718.51

WANG Li, LI Changrong, LI Fagen, ZHOU Changpin, WENG Qijie, LÜ Jiabin, CHEN Jianbo, CHEN Jiancheng, GAN Siming. SSR loci associated with population adaptation in Eucalyptus cloeziana[J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2019, 43(5): 59-66.

Figures/Tables 7

Fig.1

Fig.2

Fig.3

Fig.4

Table 1

Fig.5

Table 2

References 42

[1]	ROOT T L, PRICE J T, HALL K R, et al. Fingerprints of globalwarming on wild animals and plants[J]. Nature, 2003, 421(6918):57-60. DOI: 10.1038/nature01333. doi: 10.1038/nature01333
[2]	DAVIS M B, SHAW R G. Range shifts and adaptive responses to Quaternary climate change[J]. Science, 2001, 292(5517):673-679. DOI: 10.1126/science.292.5517.673. doi: 10.1126/science.292.5517.673
[3]	JUMP A S, PEÑUELAS J. Running to stand still: adaptation and the response of plants to rapid climate change[J]. Ecology Letters, 2005, 8(9):1010-1020. DOI: 10.1111/j.1461-0248.2005.00796.x. doi: 10.1111/ele.2005.8.issue-9
[4]	SAVOLAINEN O, LASCOUX M, MERILÄ J. Ecological genomics of local adaptation[J]. Nature Reviews Genetics, 2013, 14(11):807-820. DOI: 10.1038/nrg3522. doi: 10.1038/nrg3522
[5]	DELPH L F. The study of local adaptation: a thriving field of research[J]. Journal of Heredity, 2018, 109(1):1-2. DOI: 10.1093/jhered/esx099. doi: 10.1093/jhered/esx099
[6]	CSILLÉRY K, LALAGÜE H, VENDRAMIN G G. Detecting short spatial scale local adaptation andepistatic selection in climate-related candidate genes in European beech (Fagus sylvatica) populations[J]. Molecular Ecology, 2014, 23(19):4696-4708. DOI: 10.1111/mec.12902. doi: 10.1111/mec.12902
[7]	AITKEN SN, YEAMAN S, HOLLIDAY J A, et al. Adaptation, migration orextirpation: climate change outcomes for tree populations[J]. Evolutionary Applications, 2008, 1(1), 95-111. DOI: 10.1111/j.1752-4571.2007.00013.x. doi: 10.1111/j.1752-4571.2007.00013.x
[8]	SAVOLAINEN O, PYHÄJÄRVI T, KNÜRR T. Gene flow and local adaptation in trees[J]. Annual Review of Ecology, Evolution, and Systematics, 2007, 38:595-619. DOI: 10.1146/annurev.ecolsys.38.091206.095646. doi: 10.1146/annurev.ecolsys.38.091206.095646
[9]	KAWECKI T J, EBERT D. Conceptual issues in local adaptation[J]. Ecology Letters, 2004, 7(12):1225-1241. DOI: 10.1111/j.1461-0248.2004.00684.x. doi: 10.1111/ele.2004.7.issue-12
[10]	GIENAPP P, TEPLITSKY C, ALHO J S, et al. Climate change and evolution: disentangling environmental and genetic responses[J]. Molecular Ecology, 2008, 17(1):167-178. DOI: 10.1111/j.1365-294X.2007.03413.x. doi: 10.1111/mec.2008.17.issue-1
[11]	BRADBURY D, SMITHSON A, KRAUSS S L. Signatures of diversifying selection at EST-SSR loci and association with climate in naturalEucalyptus populations[J]. Molecular Ecology, 2013, 22(20):5112-5129. DOI: 10.1111/mec.12463. doi: 10.1111/mec.12463
[12]	SONG Z, ZHANG M, LI F, et al. Genome scans for divergent selection in natural populations of the widespread hardwood species Eucalyptus grandis ( Myrtaceae) using microsatellites[J]. Scientific Reports, 6:34941. DOI: 10.1038/srep34941. doi: 10.1038/srep34941
[13]	LIND B M, MENON M, BOLTE C E, et al. The genomics of local adaptation in trees: are we out of the woods yet[J]. Tree Genetics & Genomes, 2018, 14(2):29. DOI: 10.1007/s11295-017-1224-y.
[14]	BROOKER M I H. A new classification of the genus Eucalyptus L’Hér.(Myrtaceae)[J]. Australian Systematic Botany, 2000, 13(1):79-148. DOI: 10.1071/SB98008. doi: 10.1071/SB98008
[15]	TURNBULL J. Geographical variation in Eucalyptus cloeziana F. Muell.[D]. Canberra: Australian National University, 1979.
[16]	NGUGI M R, DOLEY D, HUNT MA, et al. Physiological responses to water stress in Eucalyptus cloeziana and E. argophloia seedlings[J]. Trees, 2004, 18(4):381-389. DOI: 10.1007/s00468-003-0316-5.
[17]	LI C, WENG Q, CHEN J, et al. Genetic parameters for growth and wood mechanical properties inEucalyptus cloeziana F. Muell.[J]. New Forests, 48(1):33-49. DOI: 10.1007/s11056-016-9554-4.
[18]	宋志姣, 杨合宇, 翁启杰, 等. 细叶桉群体的遗传多样性和受选择位点[J]. 林业科学, 2016, 52(9):39-47. DOI: 10.11707/j.1001-7488.20160905.
	SONG Z J, YANG H Y, WENG Q J, et al. Genetic diversity and selective loci in Eucalyptus tereticornis populations [J]. Scientia Silvae Sinicae, 2016, 52(9):39-47.
[19]	BRONDANI R P V, WILLIAMS E R, BRONDANI C, et al. A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus[J]. BMC Plant Biology, 2006, 6:20. DOI: 10.1186/1471-2229-6-20. doi: 10.1186/1471-2229-6-20
[20]	周长品, 李发根, 翁启杰, 等. PCR产物直接测序和混合克隆测序进行桉树EST-SSR标记开发[J]. 分子植物育种(网络版), 2010, 8(1):e1. DOI: 10.5376/mpb.cn.2010.08.0001.
	ZHOU C P, LI F G, WENG Q J, et al. Comparison between direct sequencing and pool-cloning-based sequencing of PCR products in EST-SSR marker development in Eucalyptus [J]. Molecular Plant Breeding (online), 2010, 8(1):e1.
[21]	HE X, WANG Y, LI F, et al. Development of 198 novel EST-derived microsatellites in Eucalyptus (Myrtaceae)[J]. American Journal of Botany, 2012, 99(4):e134-e148. DOI: 10.3732/ajb.1100442. doi: 10.3732/ajb.1100442
[22]	ZHOU C, HE X, LI F, et al. Development of 240 novel EST-SSRs in Eucalyptus L’Hérit.[J]. Molecular Breeding, 2014, 33(1):221-225. DOI: 10.1007/s11032-013-9923-z. doi: 10.1007/s11032-013-9923-z
[23]	LI F, GAN S. An optimised protocol for fluorescent-dUTP based SSR genotyping and its application to genetic mapping in Eucalyptus[J]. Silvae Genetica, 2011, 60(1):18-25. doi: 10.1515/sg-2011-0003
[24]	PEAKALL R, SMOUSE P. GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research[J]. Molecular Ecology Notes, 2006, 6(1):288-295. DOI: 10.1111/j.1471-8286.2005.01155.x. doi: 10.1111/men.2006.6.issue-1
[25]	HIJMANS R J, CAMERSON S E, PARRA J L, et al. Very high resolution interpolated climate surfaces for global land areas[J]. International Journal of Climatology, 2005, 25(15):1965-1978. DOI: 10.1002/joc.1276. doi: 10.1002/(ISSN)1097-0088
[26]	ANTAO T, LOPES A, LOPES R J, et al. LOSITAN: a workbench to detect molecular adaptation based on a F_st-outlier method[J]. BMC Bioinformatics, 2008, 9(1):323. DOI: 10.1186/1471-2105-9-323. doi: 10.1186/1471-2105-9-323
[27]	EXCOFFIER L, LISCHER H E L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows[J]. Molecular Ecology Resources, 2010, 10(3):564-567. DOI: 10.1111/j.1755-0998.2010.02847.x. doi: 10.1111/men.2010.10.issue-3
[28]	FOLL M, GAGGIOTTI O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective[J]. Genetics, 2008, 180(2):977-993. DOI: 10.1534/genetics.108.092221. doi: 10.1534/genetics.108.092221
[29]	STUCKI S, OROZCO-TERWENGEL P, FORESTER B R, et al. High performance computation of landscape genomic models including local indicators of spatial association[J]. Molecular Ecology Resources, 2017, 17(5):1072-1089. DOI: 10.1111/1755-0998.12629. doi: 10.1111/men.2017.17.issue-5
[30]	王莉, 李昌荣, 李发根, 等. 大花序桉SSR位点多样性和群体结构分析[J]. 分子植物育种, 2019, 17(13):4470-4478. DOI: 10.13271/j.mpb.017.004470.
	WANG L, LI C R, LI F G, et al. SSR marker diversity and population structure in Eucalyptus cloeziana [J]. Molecular Plant Breeding, 2019, 17(13):4470-4478.
[31]	HILL R S. Origins of the southeastern Australian vegetation[J]. Philosophical Transactions of the Royal Society B. Biological Science, 2004, 359(1450):1537-1549. DOI: 10.1098/rstb.2004.1526. doi: 10.1098/rstb.2004.1526
[32]	SHEPHERD M, SEXTON T R, THOMAS D, et al. Geographical and historical determinants of SSR variation in Eucalyptus pilularis[J]. Canadian Journal of Forest Research, 2010, 359(1450):1537-1549. DOI: 10.1139/X10-049.
[33]	PRUNIER J, LAROCHE J, BEAULIEU J, et al. Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce[J]. Molecular Ecology, 2011, 20(8):1702-1716. DOI: 10.1111/j.1365-294X.2011.05045.x. doi: 10.1111/mec.2011.20.issue-8
[34]	LIN Y, ZHENG H, ZHANG Q, et al. Functional profiling of EcaICE1 transcription factor gene from Eucalyptus camaldulensis, involved in cold response in tobacco plants[J]. Journal of Plant Biochemistry & Biotechnology, 2014, 23(2):141-150. DOI: 10.1007/s13562-013-0192-z.
[35]	LUKATKIN A S. Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 2. the activity of antioxidant enzymes during plant chilling[J]. Russian Journal of Plant Physiology, 2002, 49(6):782-788. DOI: 10.1023/A:1020232700648. doi: 10.1023/A:1020965629243
[36]	SAUER N. Molecular physiology of higher plant sucrose transporters[J]. FEBS Letters, 2007, 581(12):2309-2317. DOI: 10.1016/j.febslet.2007.03.048. doi: 10.1016/j.febslet.2007.03.048
[37]	NILSEN E T, MULLER W H. Phenology of the drought-deciduous shrub Lotus scoparius: climatic controls and adaptive significance[J]. Ecological Monographs, 1981, 51(3):323-341. DOI: 10.2307/2937277. doi: 10.2307/2937277
[38]	LIU Y, ZHANG T, LI X, et al. Protective mechanism of desiccation tolerance in Reaumuria soongorica: leaf abscission and sucrose accumulation in the stem[J]. Science in China Ser C: Life Sciences, 2007, 50(1):15-21.DOI: 10.1007/s11427-007-0002-8.
[39]	PLÜCKEN H, MÜLLER B, GROHMANN D, et al. The HCF136 protein is essential for assembly of the photosystem Ⅱ reaction center in Arabidopsis thaliana[J]. FEBS Letters, 2002, 532(1):85-90. DOI: 10.1016/S0014-5793(02)03634-7. doi: 10.1016/S0014-5793(02)03634-7
[40]	KOMENDA J, NICKELSEN J, TICHY M, et al. The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem Ⅱ assembly complex and is important for both the efficient assembly and repair of photosystem Ⅱ in Synechocystis sp. PCC 6803[J]. Journal of Biological Chemistry, 2008, 283(33):22390-22399. DOI: 10.1074/jbc.M801917200. doi: 10.1074/jbc.M801917200
[41]	MEURER J, PLÜCKEN H, KOWALLIK K V, et al. A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem Ⅱ in Arabidopsis thaliana[J]. EMBO Journal, 2014, 17(18):5286-5297. DOI: 10.1093/emboj/17.18.5286. doi: 10.1093/emboj/17.18.5286
[42]	SCHLÖTTERER C. Hitchhiking mapping-functional genomics from the population genetics perspective[J]. Trends in Genetics, 2003, 19(1):32-38. DOI: 10.1016/S0168-9525(02)00012-4. doi: 10.1016/S0168-9525(02)00012-4

Metrics

Comments

www.nldxb.njfu.edu.cn

Edited ＆ Published by Editorial Department of Nanjing Forestry University(Natural Sciences Edition)
Address： No.159 Longpan Road,Nanjing 210037 Jiangsu,P.R.China
E-mail ：xuebao@njfu.edu.cn , xuebao@njfu.com.cn
Telephone +86-25-85428247,85427076
Distributed by China International Book Trading Corporation P.O. Box 399, Beijing ,P.R. China

区域 region	群体 popu- lation	海拔/m altitude	气候因子climatic factors							频率/% frequency
区域 region	群体 popu- lation	海拔/m altitude	T_ma/ ℃	T_mcm/ ℃		T_mwm/ ℃		P_wq/ mm		Embra6- 118 bp		Embra20- 121 bp		EUCeSSR 298- 265 bp		EUCeSSR 676- 168 bp		EUCeSSR 1009- 179 bp		EUCeSSR 1009- 189 bp
北部 north	SC	250	24.2		16.8		30.9		932		0.0		50.0		35.7		57.1		7.1		28.6
	Bar	830	20.7		10.9		29.1		809		0.0		0.0		50.0		12.5		12.5		75.0
	Rav	1 000	19.5		8.9		28.5		661		0.0		8.3		50.0		16.7		16.7		25.0
	CarS	20	23.8		13.6		31.6		1097		20.0		5.0		55.0		50.0		10.0		40.0
	Car	6	23.9		13.8		31.6		1124		12.5		0.0		52.5		65.0		2.5		47.5
	PR	300	22.0		10.9		30.6		568		25.0		12.5		0.0		62.5		12.5		25.0
	MP	600	22.5		12.0		31.2		682		20.0		0.0		10.0		70.0		0.0		50.0
	平均 mean	429.4	22.4		12.41		30.50		839.0		11.07		10.83		36.17		47.69		8.76		41.59
南部 south	Nee	70	20.8		9.2		29.9		485		42.9		35.7		7.1		7.1		50.0		0.0
	GV	100	20.4		7.9		30.2		482		50.0		50.0		0.0		0.0		40.0		0.0
	WWP	210	20.3		8.4		29.7		513		40.0		40.0		0.0		10.0		50.0		0.0
	Wol	120	20.3		8.4		29.7		513		62.5		43.8		0.0		0.0		50.0		0.0
	TC	80	20.5		9.0		29.3		567		62.5		50.0		0.0		0.0		50.0		0.0
	Woo	400	19.6		7.9		28.9		567		66.7		44.4		11.1		0.0		33.3		5.6
	Pom	40	20.3		8.8		28.9		623		61.1		50.0		61.1		0.0		50.0		0.0
	平均 mean	145.7	20.30		8.51		29.51		535.7		55.09		44.84		11.34		2.45		46.19		0.79

SSR位点 SSR locus	等位片段/bp allele	T_ma	T_mcm	T_mwm	P_wq
Embra6	118	-	0.537 1^***	-	-
Embra20	121	-	-	-	0.382 6^***
EUCeSSR298	265	-	-	-	0.356 6^***
EUCeSSR676	168	0.662 2^***	0.661 2^***	0.621 5^***	0.496 1^***
EUCeSSR1009	179	0.523 3^***	0.590 1^***	0.457 4^***	0.535 7^***
	189	0.551 0^***	0.617 4^***	0.489 0^***	0.550 3^***

SSR loci associated with population adaptation in Eucalyptus cloeziana

RichHTML

PDF

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 7

References 42

Related Articles 13

Recommended Articles

Metrics

Comments

Author

Reader

Reviewer

[1]	LUO Chuying, SHE Jiyun, TANG Zichao. Prediction of potential distribution areas of the endangered Cathaya argyrophylla based on shared socio-economic pathways (SSPs) climate scenarios [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2024, 48(1): 161-168.
[2]	WANG Huanli, YAN Lingjun, HUANG Xi, WANG Zhongwei, TANG Shijie. Genetic diversity and genetic structure of Tilia miqueliana population [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2023, 47(1): 145-153.
[3]	LI Dandan, WENG Qijie, GAN Siming, ZHOU Changpin, HUANG Shineng, LI Mei. Identification of full-sib seedlings from an open-pollinated family of Archidendron clypearia based on EST-SSR markers [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(4): 95-101.
[4]	FENG Yining, LI Yingang, QI Ming, ZHOU Pengyan, ZHOU Qi, DONG Le, XU Li’an. Genetic diversity analyses of Phoebe bournei representative populations in Fujian Province based on SSR markers [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2022, 46(4): 102-108.
[5]	HE Xudong, ZHENG Jiwei, SUN Chong, HE Kaiyue, WANG Baosong. Construction of fingerprints for 33 varieties in Salicaceae [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2021, 45(2): 35-42.
[6]	HUANG Honglan, ZHONG Wogu, YI Deping, CAI Junhuo, ZHANG Lu. Predicting the impact of future climate change on the distribution patterns of Toona ciliata var. pubescens in China [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2020, 44(3): 163-170.
[7]	RONG Hao, HUANG Bin, ZHOU Qi, ZHANG Wangxiang, XU Li'an. The construction of fingerprints and genetic diversity analysis of 61 Malus crabapple cultivars based on SSR markers [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2018, 61(03): 45-50.
[8]	LUO Peng, CAO Yuting, MO Jiaxing, WENG Huaifeng, SHI Jisen, XU Jin. Analysis of genetic diversity and construction of DNA fingerprinting of clones in Cryptomeria fortune [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2017, 60(04): 191-196.
[9]	JIANG Dalong, XU Xia, RUAN Honghua. Review of nutrient resorption and its regulating in plants [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2017, 60(01): 183-188.
[10]	CHENG Zehu,DING Kunyuan,LIU Yanhong. Relationship between arborous layer productivity and climatic factors in Pinus tabulaeformis natural forests and plantations in Beijing [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2016, 59(05): 177-183.
[11]	ZHOU Wencai, HOU Jing, GUO Wei, CHEN Yingnan, WAN Zhibing, YIN Tongming. Identification of the true hybrids for Populus deltoides by using SSR markers [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2015, 58(03): 45-49.
[12]	OUYANG Lei, CHEN Jinhui, ZHENG Renhua, XU Yang, LIN Yufeng, HUANG Jinhua, YE Daiquan, FANG Yanghui, SHI Jisen. Genetic diversity among the germplasm collections of the Chinese fir in 1^st breeding population upon SSR markers [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 2014, 57(01): 21-26.
[13]	Ye Zhihong Shi Jisen Weng Yuzhen Li Shaumao Yu Rongzhou Chen Renxian (Nanjing Forestry University). GEOGRAPHIC VARIATION AND INHERITANCE, CORRELATION AND SELECTION OF TRAITS OF PROVENANCES OF CHINESE FIR [J]. JOURNAL OF NANJING FORESTRY UNIVERSITY, 1991, 34(02): 7-10.