NEW INSIGHTS INTO THE PHYLOGENY AND SPECIATION OF KUMQUAT (<i>FORTUNELLA</i> SPP.) BASED ON CHLOROPLAST SNP, NUCLEAR SSR AND WHOLE-GENOME SEQUENCING

doi:10.15302/J-FASE-2021436

Front. Agr. Sci. Eng.

2022, Vol. 9

Issue (4) : 627-641 https://doi.org/10.15302/J-FASE-2021436

RESEARCH ARTICLE

NEW INSIGHTS INTO THE PHYLOGENY AND SPECIATION OF KUMQUAT (FORTUNELLA SPP.) BASED ON CHLOROPLAST SNP, NUCLEAR SSR AND WHOLE-GENOME SEQUENCING

Chenqiao ZHU¹, Peng CHEN¹, Junli YE¹, Hang LI^1,², Yue HUANG¹, Xiaoming YANG¹, Chuanwu CHEN^1,³, Chenglei ZHANG¹, Yuantao XU¹, Xiaoli WANG^1,⁴, Xiang YAN⁴, Guangzhou DENG³, Xiaolin JIANG¹, Nan WANG¹, Hongxing WANG¹, Quan SUN¹, Yun LIU¹, Di FENG¹, Min YU¹, Xietian SONG¹, Zongzhou XIE¹, Yunliu ZENG¹, Lijun CHAI¹, Qiang XU¹, Chongling DENG³, Yunjiang CHENG¹, Xiuxin DENG¹(

)

¹. Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan 430070, China
². Fruit Industry Technology Guidance Stand of Ganzhou, Ganzhou 341000, China
³. Guangxi Academy of Specialty Crops/Guangxi Citrus Breeding and Cultivation Research Center of Engineering Technology, Guilin 541004, China
⁴. Ganzhou Citrus Research Institute, Ganzhou 341000, China

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Abstract

● Fortunella genus consists of two populations: cultivated kumquat and wild Hong Kong kumquat.

● Artificial selection might involve in the origin of cultivated Fortunella species.

● A hypothesis for the differentiation and speciation of Fortunella species is proposed.

Kumquat (Fortunella spp.) is a fruit and ornamental crop worldwide due to the palatable taste and high ornamental value of its fruit. Although Fortunella is classified into the economically important true citrus fruit tree group together with Citrus and Poncirus, few studies have been focused on its evolutionary scenario. In this study, analysis of five chloroplast loci and 47 nuclear microsatellites (nSSR) loci from 38 kumquat and 10 citrus accessions revealed the independent phylogeny of Fortunella among citrus taxa, and that Fortunella mainly comprises two populations: CUL, cultivated Fortunella spp. (F. margarita, F. crassifolia and F. japonica); and HK, wild Hong Kong kumquat (Fortunella hindsii). Genomic analysis based on whole-genome SNPs indicated that the allele frequency of both pupations deviated from the neutral selection model, suggesting directional selection was a force driving their evolutions. CUL exhibited lower genomic diversity and higher linkage strength than HK, suggesting artificial selection involved in its origin. A high level of genetic differentiation (Fst = 0.364) was detected and obviously asynchronous demographic changes were observed between CUL and HK. Based on these results, a new hypothesis for the speciation of Fortunella is proposed.

Keywords Citrus Fortunella kumquat phylogenetics

Corresponding Author(s): Xiuxin DENG

Just Accepted Date: 18 March 2022 Online First Date: 11 April 2022 Issue Date: 07 November 2022

Cite this article:

Chenqiao ZHU,Peng CHEN,Junli YE, et al. NEW INSIGHTS INTO THE PHYLOGENY AND SPECIATION OF KUMQUAT (FORTUNELLA SPP.) BASED ON CHLOROPLAST SNP, NUCLEAR SSR AND WHOLE-GENOME SEQUENCING[J]. Front. Agr. Sci. Eng. , 2022, 9(4): 627-641.

URL:

https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2021436
https://academic.hep.com.cn/fase/EN/Y2022/V9/I4/627

Accession code	Common name	Species	Location	Description	Utilization
LF	Nagami	Fortunella margarita	Taizhou, Zhejiang	Germplasm	1, 2, 3
QZLF	Nagami	F. margarita	Quzhou, Zhejiang	Germplasm	1, 2
DGLF	Nagami	F. margarita	Zhejiang	Landrace	1, 2, 3
JZLF	Nagami	F. margarita	Zhejiang	Landrace	1, 2
WZLF	Nagami	F. margarita	Wenzhou, Zhejiang	Landrace	1, 2
LFHY	Nagami	F. margarita	Taizhou, Zhejiang	Landrace	1, 2
LW	Narumi	F. japonica	Ningbo, Zhejiang	Germplasm	1, 2, 3
GXCP	Narumi	F. japonica	Liuzhou, Guangxi	Landrace	1, 2, 3
LCHP	Meiwa	F. crassifolia	Guilin, Guangxi	Cultivar	1, 2
HPJG	Meiwa	F. crassifolia	Guilin, Guangxi	Landrace	1, 2, 3
LSHY	Meiwa	F. crassifolia	Yongzhou, Hunan	Germplasm	1, 2
YXBZQ	Meiwa	F. crassifolia	Sanming, Fujian	Landrace	1, 2, 3
JX4	Meiwa	F. crassifolia	Ji’an, Jiangxi	Cultivar	1, 2, 3
LYJD	Meiwa	F. crassifolia	Changsha, Hunan	Germplasm	1, 2, 3
WZJD	Meiwa	F. crassifolia	Wenzhou, Zhejiang	Germplasm	1, 2, 3
LSJG	Meiwa	F. crassifolia	Yongzhou, Hunan	Landrace	1, 2, 3
LYJG	Meiwa	F. crassifolia	Changsha, Hunan	Cultivar	1, 2
NBJD	Meiwa	F. crassifolia	Ningbo, Zhejiang	Cultivar	1, 2
RAJG	Meiwa	F. japonica	Liuzhou, Guangxi	Landrace	1, 2, 3
YSJG	Meiwa	F. crassifolia	Guilin, Guangxi	Cultivar	1, 2, 3
G1	Meiwa	F. crassifolia	Guilin, Guangxi	Landrace	1, 2
G2	Meiwa	F. crassifolia	Guilin, Guangxi	Landrace	1, 2, 3
DJD	Hong Kong	F. hindsii	Fujian	Ornamental	1, 2
XJD	Hong Kong	F. hindsii	Fujian	Ornamental	1, 2
WTD	Hong Kong	F. hindsii	Jieyang, Guangdong	Wild	1, 2, 3
JD	Hong Kong	F. hindsii	Fujian	Ornamental	1, 2
DR01	Hong Kong	F. hindsii	Longyan, Fujian	Wild	1, 2, 3
DB02	Hong Kong	F. hindsii	Ganzhou, Jiangxi	Wild	1, 2, 3
CZ	Hong Kong	F. hindsii	Chenzhou, Hunan	Wild	1, 2, 3
MJS	Hong Kong	F. hindsii	Ningbo, Zhejiang	Wild	1, 2, 3
WGJ	Wenguangju	Hybrid	/	Ornamental	1, 2
JGZ	/	Hybrid	/	Rootstock	1, 2
SJJ	Calamondin	Citrus madurensis	Fujian	Cultivar	1, 2
CS	Changshou	F. obovata	Fujian	Ornamental	1, 2
HCYJG	Meiwa	F. crassifolia	Ganzhou, Jiangxi	Germplasm	1, 2, 3
XLF	Nagami	F. margarita	Ningbo, Zhejiang	Landrace	1, 2, 3
YXJG	Meiwa	F. crassifolia	Sanming, Fujian	Cultivar	1, 2
YCJD	Meiwa	F. crassifolia	Quanzhou, Fujian	Germplasm	1, 2
ML	Lime	C. aurantifolia	/	Cultivar	1, 2
XC	Sweet orange	C. sinensis	/	Cultivar	1, 2
ZHI	Trifoliate orange	Poncirus	/	Cultivar	1, 2
XY	Foshou citron	C. medica	/	Cultivar	1, 2

YCC	Papeda	C. ichangensis	/	Wild	1, 2
GXMY	Pummelo	C. maxima	/	Cultivar	1, 2
MSYJ	Mandarin	C. reticulata	/	Cultivar	1, 2
HKC	Box orange	Atalantia	/	Relatives	1, 2
NM	Lemon	C. limon	/	Cultivar	1, 2
SC	Sour orange	C. aurantium	/	Cultivar	1, 2
CFX	Hong Kong	F. hindsii	Ganzhou, Jiangxi	Wild	3
JIEX	Hong Kong	F. hindsii	Jieyang, Guangdong	Wild	3
DYS02	Hong Kong	F. hindsii	Sanming, Fujian	Wild	3
LH08	Hong Kong	F. hindsii	Xiamen, Fujian	Wild	3
DYT01	Hong Kong	F. hindsii	Longyan, Fujian	Wild	3
ZX9	Hong Kong	F. hindsii	Wenzhou, Zhejiang	Wild	3
LY43	Hong Kong	F. hindsii	Ningbo, Zhejiang	Wild	3
HC27	Hong Kong	F. hindsii	Shaoguan, Guangdong	Wild	3
XMS	Hong Kong	F. hindsii	Guangzhou, Guangdong	Wild	3
JLS	Hong Kong	F. hindsii	Ganzhou, Jiangxi	Wild	3

Tab.1 Details and utilization of the accession evaluated in this study

Fig.1 Phylogenetic tree and haplotype network of Fortunella based on five chloroplast loci. (a) Phylogenetic tree of 38 Fortunella and 10 citrus accessions. Clades of the tree are highlighted by different colors. Clade I, black, Chinese box orange (Atalantia buxifolia); Clade II, yellow, citron (Citrus medica); Clade III, light green, lime (C. aurantiifolia), papeda (C. ichangensis) and wild mandarin (C. reticulata); Clade IV, dark green, trifoliate orange (Poncirus trifoliata); Clade V, olive, sweet orange (C. sinensis), lemon (C. limon), pummelo (C. maxima) and sour orange (C. aurantium); and Clade VI, red, kumquat (Fortunella spp.). (b) Haplotype network of 38 Fortunella and 10 citrus accessions. Each dot on the network presents a type of haplotype. The genera are: blue, Poncirus; yellow, Citrus; black, Atalantia; and red, Fortunella. (c) Composition of the 11 Fortunella haplotypes. Species are highlighted as: purple, Hong Kong kumquat (F. hindsii); blue, Meiwa kumquat (F. crassifolia); salmon, Nagami kumquat (F. margarita); green, Marumi kumquat (F. japonica); and gray, hybrid kumquat.

Fig.2 Genetic structure of 38 kumquat and 10 citrus accessions based on 47 nSSR loci. (a)Principal component analysis of 38 kumquat and 10 citrus accessions. Accessions are presented by different colors (as in Fig. 1(a)). Clade I, black, Chinese box orange (Atalantia buxifolia); Clade II, yellow, citron (Citrus medica); Clade III, light green, lime (C. aurantiifolia), papeda (C. ichangensis) and wild mandarin (C. reticulata); Clade IV, dark green, trifoliate orange (Poncirus trifoliata); Clade V, olive, sweet orange (C. sinensis), lemon (C. limon), pummelo (C. maxima) and sour orange (C. aurantium); Clade VI, red, kumquat (Fortunella spp.). (b) Phylogenetic tree and population structure of 38 kumquat and 10 citrus accessions based on nSSR data. On the left side, phylogenetic tree was constructed using distance-based UPGMA method; clades of known kumquat hybrids (WGJ, CS, JGZ and Calamondin), cultivated Fortunella spp. (F. margarita, F. crassifolia and F. japonica) and Hong Kong kumquat (F. hindsii) accessions are shown in pink, orange and green, respectively. On the right side, each accession is represented by a horizontal stacked bar of genetic components with the proportion shown in color for K = 2 estimated by STRUCTURE.

Fig.3 Phenotype and population structure of cultivated Fortunella spp. (CUL) and wild Hong Kong kumquat (HK). (a) Fruit phenotypes of the four Fortunella spp. (b) Cross and longitudinal sections of CUL and HK; CUL has larger fruit organ with thickened and sweet albedo, whereas HK has smaller fruit with thin and acerb peel. (c) Population structure among 15 CUL and 15 HK accessions based on whole-genomic 5,104,141 SNPs. Each accession is represented by a vertical stacked column of genetic components with the proportion shown in color for K = 2, 3 and 4 estimated by ADMIXTURE.

Tab.2 Genomic diversity of cultivated Fortunella (CUL) and wild Hong Kong kumquat (HK) populations

Tab.3 Genomic divergence between cultivated Fortunella (CUL) and wild Hong Kong kumquat (HK) populations

Fig.4 Demographic history and speciation hypothesis of Fortunella. (a) Demographic history of cultivated Fortunella (CUL) and wild Hong Kong kumquat (HK) populations. Effective population size of the CUL (orange curve) and HK (green curve) were reconstructed by using the pairwise sequentially Markovian coalescent model. Quaternary glacial period is marked by blue background. Obvious population bottlenecks are marked by gray background. (b) Speciation hypothesis of Fortunella spp. Blue, orange and green dots represent the common ancestor of Fortunella, cultivated Fortunella spp. (F. margartita, F. crassifolia and F. japonica) and Hong Kong kumquat (F. hindsii) populations, respecitvely. The peaked line represents geographical barrier; straight arrow represents natural selection; dotted arrow indicates artificial selection. The northern population experienced earlier and severer climatic changes during Quaternary glacial period (QGP) compared to the southern population. During QGP, the northern and southern populations were gradually isolated from each other by geographical barrier (probably Nanling Mountains) and underwent adaptive evolution separately. With the southward migration of humans, modern cultivated Fortunella spp. were selected from the northern population.

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[1]	Manosh Kumar BISWAS, Christoph MAYER, Xiuxin DENG. *Repeats in the transcribed regions: comprehensive characterization and comparison of Citrus* spp.**[J]. Front. Agr. Sci. Eng. , 2017, 4(4): 421-432.

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