Kalita Et Al (2021)

Perspectives in Plant Ecology, Evolution and Systematics 53 (2021) 125644
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Perspectives in Plant Ecology, Evolution and Systematics

journal homepage: www.elsevier.com/locate/ppees
A molecular perspective on the taxonomy and journey of

Citrus domestication
Barsha Kalita a, Abhijeet Roy a, A. Annamalai b, Lakshmi PTV a, *
a
Department of Bioinformatics, School of Life Sciences, Pondicherry University, Puducherry, 605 014, India
b
PG and Research Department of Botany, Arignar Anna Government Arts College, Villupuram, Tamil Nadu, 605 602, India
A R T I C L E I N F O A B S T R A C T
Keywords: The highly-demanded commercial citrus fruits of family Rutaceae arose primarily through sexual hybridization
Citrus origin between the four ancestral taxa generating a range of nothospecies. The diversity of phenotypic traits in these
Hybridization cultivable groups was mainly due to somatic mutations fixed either by apomixis present in Citrus species or
Molecular phylogeny
grafting for clonal propagation, leaving behind very scanty evidence to study the process of citrus domestication
Apomixis
Self-incompatibility
apart from its genealogy. Moreover, sexual compatibility between Citrus and its related genera is another broad
Citrus domestication area of controversy leading to a continuous reformulation of citrus taxonomy and phylogeny. Although advanced
genomic studies to clarify the phylogenetic relationships of citrus are in progress, a detailed overview of citrus
taxonomy, diversity, origin and domestication would enhance our knowledge not only to get an evolutionary
framework of citrus phylogeny but also to unravel the history of citrus domestication. Therefore, the review has
been presented comprehensively with recent studies emphasizing the identification of specific reproductive,
sensory and morphological markers selected as traits during the course of domestication. Hence, studies on
identifying genes related to polyembryony, self-incompatibility (SI) and anthocyanin production between wild
and cultivated citrus have been discussed to provide new insights on citrus apomixis, SI and citric acid reduction.
Further, the correlation of pummelo introgression with fruit size and palatability in cultivable mandarins has also
been focused on understanding mandarin domestication.
1. Introduction (12.86 %) and grapefruit (6.70 %). Apparently, China alone contributed
to 26 % among the topmost citrus fruits producing countries followed by
The genus Citrus, grown widely from tropical to subtropical areas of Brazil (13 %), India (8%), U.S.A (6%), Spain (5.5 %) and Mexico (5.3 %)
the world, is an important fruit crop known for its refreshing fragrance, (http://www.fao.org/economic/est/est-commodities/citrus-fruit/en/).
abundance of vitamin C content and health-promoting values (Khan Despite the popularity of citrus fruits (oranges, mandarins, lemons,
et al., 2014). The bioactive compounds responsible for its nutraceutical limes, grapefruits etc.), a clear picture of their taxonomic distribution
and anti-microbial properties, including phenolic compounds (mostly and domestication process remains unresolved. Therefore, to breed high
flavonoids), carotenoids, terpenoids, vitamins, minerals etc. (Abey quality and new variety of citrus fruits, it is important to have in-depth
singhe et al., 2007), are reported to be associated with the decreased risk knowledge about the relationships of the different taxa within the Cit
against cancer, cardiovascular and neuronal damages (Li and Schlues reae tribe perhaps not only to improve better breeding strategies but also
ener, 2017), oxidative stress and inflammations (Chen et al., 2017), to advance conservation strategies for the wild taxa. However, taxon
diabetes (Testa et al., 2016), obesity (Nakajima et al., 2014) etc., and omy and phylogeny of citrus are often debated due to recurring
active against pathogens like bacteria, viruses and fungi (Orhan et al., cross-pollination and phenomenon like- nucellar polyembryony that
2010). Therefore, there is a huge demand for citrus fruits across the becomes stable and continues in the hybrid taxa (Scora, 1975). Further,
globe and as estimated by Food and Agriculture Organizations of the assigning the rank of a species becomes questionable due to their
United Nations (FAO) 2017, the world production of citrus has reached disparity on the degree of divergence justifying a species status. How
approximately 124.25 million tonnes with the leading varieties of or ever, molecular marker technologies have clarified some of these re
anges (53.90 %), followed by tangerines (26.53 %), lemons and limes lationships, which later became much easier with the development of
* Corresponding author.
E-mail address: lakanna@bicpu.edu.in (L. PTV).
https://doi.org/10.1016/j.ppees.2021.125644
Received 9 July 2021; Received in revised form 24 September 2021; Accepted 4 October 2021
Available online 7 October 2021
1433-8319/© 2021 Elsevier GmbH. All rights reserved.
B. Kalita et al. Perspectives in Plant Ecology, Evolution and Systematics 53 (2021) 125644
whole genome sequencing techniques on both nuclear and chloroplast 3. Phylogeny of ancestral and modern varieties within citrus
genomes that inferred the parentage among different citrus varieties and
deduced the patterns of admixture varieties to confirm their hybrid or Over the last century, many classification systems for citrus taxon
igins. Hence, molecular studies on Citrus species now focus on the genes omy have been proposed based on geographical and morphological
involved in the domestication process to understand the genetic basis of data. Among these, two important but distinct systems by Swingle and
selecting desirable traits. Therefore, to develop a better variety of citrus Reece (1967) and Tanaka (1977) have gained immense popularity and
fruits, understanding citrus taxonomy, phylogeny and genetic vari were widely accepted. Their classification systems were based on the
ability is crucial. Thus, the present review summarizes the information species number they recognized, while Swingle reported only 16 species
on citrus taxonomy, phylogeny, origin and domestication. In the sub in the genus Citrus; on the other hand, 162 Citrus species were identified
sequent sections, Citrus represents the genus and its species whereas by Tanaka. For instance, different mandarin varieties were designated as
non-italicized term represents citrus fruits in general. C. reticulata by Swingle, whereas Tanaka assigned individual mandarin
varieties with distinct scientific names considering them as individual
2. Citrus taxonomy and controversy species. Perhaps, the difficulties in species recognition in the case of
agamous plants, as demonstrated by Stebbins (1950) and Lawrence
The genus Citrus belongs to the subfamily Aurantioideae of Rutaceae, (1951), was known and considered by Swingle and Reece, resulting in
which was previously placed in the order Geraniales (Davies and reduced species number in their system. Later, biochemical and different
Albrigo, 1994) is now placed in Sapindales (https://www.ncbi.nlm.nih. molecular techniques were employed to decipher the taxonomic posi
gov/Taxonomy/Browser/wwwtax.cgi; http://www.mobot.org/MOBO tion in Citrus species:
T/research/APweb/). The subfamily Aurantioideae has two tribes-
Clauseneae (5 genera) and Citreae (28 genera), of which the tribe Cit 3.1. Biochemical and hybridization-based marker studies
reae is divided into three subtribes. The subtribe- Citrinae includes three
groups: the ‘primitive citrus fruit trees’, the ‘near citrus fruit trees’ and Based on biochemical data, Scora (1975), for the first time, put forth
the ‘true citrus fruit trees’ of which the last group is valued for its eco the names of three hypothetical taxa, i.e., pummelo (C. maxima (Burm.)
nomic and nutritional benefits represented by the genus Citrus and its Merr., formerly C. grandis), mandarin (C. reticulata Blanco) and citron
closely related genera: Fortunella, Poncirus, Microcitrus, Eremocitrus and (C. medica L.) referring them as the three ‘basic species’ to be the an
Clymenia (Swingle and Reece, 1967; Krueger and Navarro, 2007). cestors of cultivated citrus and published a novel work proposing
Further, Swingle and Reece (1967) classified the genus Citrus into two modern varieties (oranges, grapefruits, lemons and limes) to arise from
subgenera, Papeda and Citrus, by comparing their petiole wing’s width frequent hybridization among these ancestors. At the same time, this
with the leaflets and the presence of acridic oil in these fruits. hypothesis was also supported by a numerical taxonomic work empha
The genus Fortunella includes four species (F. japonica (Thunb.) sizing the essential biological criteria (free gene exchange, reproductive
Swingle, F. margarita (Lour.) Swingle, F. polyandra (Ridl.) Tanaka and isolation etc.) that were met by pummelo, mandarin and citron for their
F. hindsii (Champ. ex Benth.) Swingle (Swingle, 1943) and two hybrid consideration as the ‘true basic species’(Barrett and Rhodes, 1976).
taxa (F. obovata Tanaka, F. crassifolia Swingle) (Fantz, 1988). Fortunella Thereafter, the role of these three taxa for the origin of cultivable vari
species originated in northern China, and its fruits are commonly known eties was further examined and confirmed through protein electropho
as kumquats. The genus Poncirus also originated in northern China. resis (Handa et al., 1986), isozyme marker (Herrero et al., 1996a;
Earlier, it was considered to be monotypic (P. trifoliata (L.) Raf.), but 1996b) and restriction fragment length polymorphism (RFLP) (Federici
later in the 1980s, P. polyandra reported in Yunnan, China, contributed et al., 1998). Thus, sweet and sour oranges were speculated to arise from
to this genus as another new species (Ding et al., 1984). Poncirus has few hybridization between mandarin and pummelo, while a cross between
distinct characters that differ from the rest of the species of ‘true citrus citron and lime was predicted for the origin of lemons (Scora, 1975;
fruit trees’ group, such as trifoliate leaves and deciduous behaviour with Barrett and Rhodes, 1976).
high tolerance to cold (-20 ◦ C). The genera Microcitrus and Eremocitrus
are Australian in origin and closely related (Bayer et al., 2009), where 3.2. PCR markers and NGS based studies
Eremocitrus, a monospecific genus (E. glauca (Lindl.) Swingle) is known
to be cold-tolerant and xerophytic, while Microcitrus is considered DNA markers are more informative and unaffected by environmental
semixerophytic (Swingle and Reece, 1967). Clymenia, the most distinc factors in comparison to morphological data. Therefore, various mo
tive and primitive genus of all the related genera, is native to New lecular markers such as randomly amplified polymorphic DNA (RAPD)
Guinea and has edible fruits resembling those of sweet limes (Lu et al., (Federici et al., 1998; Nicolosi et al., 2000) and sequence characterized
2011; Ollitrault et al., 2020). Even though all these five related genera of amplified region (SCAR) (Nicolosi et al., 2000), enabled to reveal a
Citrus (Fortunella, Poncirus, Microcitrus, Eremocitrus and Clymenia) show fourth species viz. C. micrantha (a wild Papeda species) in addition to
considerable morphological differentiation still are sexually compatible those three ancestral species. They found most of the limes and lemons
with each other (Krueger and Navarro, 2007), making the classification to be included in the papeda cluster and confirmed it to be an additional
of Citrus species very difficult for taxonomists. Moreover, the taxonomic species responsible for the origin of presently cultivated citrus. Another
classification of Citrus species becomes even more complex due to the PCR based marker, simple sequence repeats (SSRs), helped in
presence of a remarkable feature of nucellar polyembryony- a special strengthening the studies of citrus phylogeny due to its polymorphic and
type of apomixis where the development of embryos occur from somatic co-dominant nature together with less time consuming and
nucellar cells (Batygina and Vinogradova, 2007). The probability of labour-intensive ability (Cheng et al., 2005; Barkley et al., 2006; Luro
selection and dispersal of these nucellar embryos is greater than the et al., 2008; Ollitrault et al., 2010; Biswas et al., 2014; Shimizu et al.,
usual zygotic embryos in cases of competition for germination and 2016). However, Barkley et al. (2009) evidenced that the concept of
growth. Hence, the apomictic line gets fixed and established among the homoplasy might limit the scope of SSRs as markers to demonstrate the
commercial citrus fruits like mandarins, sweet oranges, grapefruits, citrus phylogenetic origin. Eventually, the use of single nucleotide
lemons and limes considered as modern-day cultivable citrus varieties polymorphisms (SNPs) (Novelli et al., 2004; Dong et al., 2010; Ollitrault
(Kepiro and Roose, 2009). Additionally, the long history of cultivation, et al., 2012; Garcia-Lor et al., 2013), insertions/deletions (InDels)
repeated cross pollination and high frequency of bud mutations had (Ollitrault et al., 2012), a mix of InDels-SSRs (García-Lor et al., 2012;
complicated the taxonomic and phylogenetic relationships of the true Shimizu et al., 2016) and InDels-SSRs-SNPs (Curk et al., 2016; Gar
Citrus species (Nicolosi et al., 2000). Thus, these features within the cia-Lor et al., 2013; Ollitrault et al., 2015) were all found to be more
genus Citrus necessitate investigation to ensure its origin and phylogeny. suitable and efficient species diagnostic markers which helped in
2
deciphering the role of the four main ancestral taxa (mandarin, (Barkley et al., 2006) and sequence related amplified polymorphism
pummelo, citron and papeda) to the origin of cultivable Citrus species. (SRAP) (Uzun et al., 2009) markers were also in agreement with this
With the advancement in DNA sequencing technology, remarkable view of sweet oranges to have a greater allele proportion from manda
progress was made with genomic resources. Subsequently, chloroplast rins in contrast to the RAPD and SCAR marker analyses by Nicolosi et al.
and mitochondrial genome sequences of sweet orange (Bausher et al., (2000), who suggested for an equal contribution from each parent.
2006; Yu et al., 2018) and chloroplast genome of Omami lime (Su et al., Maternal phylogenetic studies using chloroplastic (Bayer et al., 2009)
2014) were released, followed by repositories of whole genome se and mitochondrial (Froelicher et al., 2011) genomes revealed pummelo
quences of other important Citrus species (Xu et al., 2013; Wu et al., as a female parent of sweet oranges. Later, the release of the complete
2014, 2018; Wang et al., 2017, 2018). These whole genome sequencing draft genome of sweet orange showed its high (50 %) heterozygosity rate
data allowed using powerful informative markers like SNPs and InDels, and confirmed the 1:3 genetic input ratio from pummelo and mandarin,
which, together with studies like genotyping by sequencing (GBS), respectively (Xu et al., 2013).
helped to identify and analyze genomes of hybrids and admixed vari
eties to trace the gap of the genealogy of some of the commercial citrus Modern admixed mandarin
cultivars, i.e., sour orange, sweet orange, grapefruit, Mexican lime, It is interesting to note that most commercially available modern
lemon, bergamot, Rangpur lime and rough lemons. mandarins are actually not genetically pure mandarin varieties and
The overall genealogy of ancestral and modern varieties is depicted should not be confused with the wild ancestral C. reticulata (mandarin)
in Fig. 1 and the various classification systems proposed for Citrus spe species. This breakthrough analysis was revealed through whole-
cies in Table 1. genome sequencing (WGS) work of Wu et al. (2014), who evidenced a
substantial admixture of pummelos in all the observed mandarin ge
Sour orange (C. aurantium L.) nomes suggesting those mandarins not to be of pure C. reticulata
Sour orange was presumed to be a natural hybrid from a direct cross (mandarin) genome but rather having introgressed fragments from
between mandarin and pummelo (Nicolosi et al., 2000; Barkley et al., pummelo genomes. This WGS work was confirmed with stronger sup
2006; Luro et al., 2008). Structure analysis using SSR (García-Lor et al., port through genotyping by sequencing (GBS) study, where a wider set
2012) and SNP (Ollitrault et al., 2012) markers revealed a higher of mandarin collections previously considered as pure C. reticulata
mandarin gene pool contribution in sour oranges than from pummelo (mandarin) types showed pummelo introgressions (Oueslati et al.,
gene pool. Later, whole-genome sequencing data concluded sour orange 2017). Recently, Wu et al. (2018) proposed a framework for
as a direct F1 interspecific hybrid between pummelo as a female parent admixture-based classification to deduce the line of pummelo admixture
and pollen of a wild mandarin (Wu et al., 2014, 2018; Oueslati et al., in the mandarin gene pool and classified mandarins into three types
2017). Further, structure analysis using SNP data by Curk et al. (2015) based on the presence or absence of shared-haplotypes across the ge
inferred almost a 50 % contribution from each of the two parent species. nomes of twenty-eight observed mandarins. Thus, among the total
mandarins, five (Sun Chu Sha Kat, Tachibana and three Chinese man
Sweet orange (C. sinensis (L.) Osbeck) darins without names) were included under type I/ pure mandarin
Unlike sour oranges, the origin of sweet orange was found to be more showing no interspecific admixture in their C. reticulata genomes,
complex considering it as a backcross product (pummelo x mandarin) x sixteen mandarins (such as Ponkan, Sunki, Cleopatra, Willowleaf,
mandarin with 75 % genetic makeup from mandarin and 25 % from Huanglingmiao, Dancy, Changsha and nine Chinese unnamed manda
pummelo (García-Lor et al., 2012). Previous studies based on SSR rins) were grouped as type II/ early admixture mandarin with short
Fig. 1. Genealogy of cultivable Citrus species.

(The coloured box encloses the names of four ancestral species: citron (C. medica), mandarin (C. reticulata), papeda (C. micrantha) and pummelo (C. maxima) with
their contribution as male and female species during hybridization and introgression event. Fruit images are not to be scaled. Adapted from Curk et al. (2016) and Wu
et al. (2018).
3
Table 1
Comparison of earlier taxonomic classifications and current phylogenomic classification for Citrus species with common names and their hybrid types.
Sl. Common Name Current Bhattacharya and Tanaka (1961) Swingle and Zhang and Pure/Hybrid type Phylogenomic
No. phylogenomic Dutta (1956)* Reece (1967) Mabberley references
name (2008)
1. Pummelo Citrus maxima Citrus maxima (L.) Citrus maxima Citrus maxima Citrus maxima Pure type Curk et al., 2015; Wu
(Burm.) Merr. Merr. et al., 2018
2 Small flowered/ Citrus micrantha Citrus micrantha Citrus Citrus hystrix Pure type Curk et al., 2015, 2016;
small fruited Wester micrantha DC. Wu et al., 2018
Papeda
3. Tachibana Citrus reticulata Citrus tachibana Citrus Citrus reticulata Pure mandarin/ Wu et al., 2018
mandarin var. (Makino) tachibana Type 1 mandarin
tachibana ined. Tanaka
4. Sun-Chu-Sha- Citrus reticulata Citrus reticulata Citrus reticulata Pure mandarin/ Wu et al., 2018
Kat mandarin var. var. austera Blanco Type 1 mandarin
austera Swingle
5. Willowleaf Citrus × Citrus deliciosa Citrus reticulata Citrus reticulata Early admixed/ Wu et al., 2014, 2018;
mandarin aurantium var. Ten. Type 2 mandarin Curk et al., 2015;
deliciosa ined. Oueslati et al., 2017
6. Dancy mandarin Citrus × Citrus tangerina Citrus reticulata Citrus reticulata Early admixed/ Curk et al., 2015;
aurantium var. hort. ex Tanaka Type 2 mandarin Oueslati et al., 2017; Wu
tangerina ined. et al., 2018
7. Clementine Citrus × Citrus clementina Citrus reticulata Late admixed/ Wu et al., 2014, 2018;
aurantium var. hort. ex Tanaka Type3 mandarin Curk et al., 2015;
clementina ined. Oueslati et al., 2017
8. King mandarin Citrus × Citrus nobilis Lour. Citrus nobilis Citrus reticulata Citrus × Late admixed/ Curk et al., 2015;
aurantium var. Lour. hybrid aurantium Type3 mandarin Oueslati et al., 2017; Wu
nobilis ined. et al., 2018
9. Satsuma Citrus × Citrus unshiu Citrus reticulata Citrus reticulata Late admixed/ Curk et al., 2015;
mandarin aurantium var. Marcow. clone Type3 mandarin Oueslati et al., 2017; Wu
unshiu ined. et al., 2018
10. Citron Citrus medica L. Citrus medica L. Citrus medica Citrus medica Citrus medica Pure type Curk et al., 2015, 2016;
Wu et al., 2018
11. Sour orange Citrus × Citrus aurantium L. Citrus aurantium Citrus Citrus × Hybrid (C. maxima Wu et al., 2014, 2018;
aurantium aurantium aurantium x C. reticulata) Curk et al., 2015;
L. var. aurantium Oueslati et al., 2017
12. Sweet orange Citrus × Citrus sinensis L. Citrus sinensis Citrus sinensis Citrus × Hybrid (C. maxima Wu et al., 2014, 2018;
aurantium var. (L.) aurantium x admixed Curk et al., 2015;
sinensis L. Osbeck C. reticulata) Oueslati et al., 2017
13. Grapefruit Citrus × Citrus paradisi Citrus paradisi Citrus × Hybrid (C. maxima Curk et al., 2015;
aurantium var. Macfad. aurantium x C. sinensis) Oueslati et al., 2017; Wu
paradisi ined. et al., 2018
14. Lemon Citrus × limon Citrus limon (L.) Citrus limon (L.) Citrus limon Citrus × limon Hybrid (C. medica x Curk et al., 2016; Wu
var. Burm. f. Burm. f. C. aurantium) et al., 2018
limon (L.) Burm. f.
15. Bergamot Citrus × limon Citrus bergamia Citrus Citrus × limon Hybrid (C. limon x Curk et al., 2016
var. Risso and Poit. aurantiifolia C. aurantium)
bergamia ined.
16. Lime Citrus × Citrus aurantiifolia Citrus Citrus Citrus × Hybrid (C. medica x Curk et al., 2016; Wu
aurantiifolia (Christm.) Swingle aurantiifolia aurantiifolia aurantiifolia C. micrantha) et al., 2018
var. aurantiifolia
17. Alemow Citrus × Citrus Citrus Hybrid (C. medica x Curk et al., 2016
aurantiifolia macrophylla aurantiifolia C. micrantha)
var. macrophylla Wester (Christm.)
ined. Swingle
18. Adam’s apple Citrus × Citrus aurata Citrus limon Citrus × Hybrid (C. medica x Curk et al., 2016
aurantiifolia Risso (L.) aurantium L. C. micrantha)
var. aurata ined. Burm. f.
19. Rangpur lime Citrus × limonia Citrus limonia Citrus limon Hybrid (C. medica x Curk et al., 2016; Wu
Osbeck var. C. reticulata) et al., 2018
limonia
20. Rough lemon Citrus × limonia Citrus jambhiri Citrus jambhiri Citrus limon Citrus × Hybrid (C. medica x Curk et al., 2016; Wu
var. Lush. Lush. taitensis Risso C. reticulata) et al., 2018
jambhiri ined.
21. Khatta Kharna Citrus × limonia Citrus karna Raf. Citrus karna Raf. Hybrid (C. medica x Curk et al., 2016
lime Osbeck var. C. reticulata)
limonia
*
taken from Stone B.C (1994).
segments (1–10 % length of the genetic map) of pummelo introgressions pummelo haplotypes to form the type II mandarins. Later, few addi
while seven mandarins (Clementine, King, Fallglo, W. Murcott, Wilking, tional pummelo introgressions finally resulted in type III mandarins as
Satsuma and Kiyomi) formed type III/ late admixture mandarin with well as sweet oranges, thus, indicating that most of today’s type III
longer (12–38 %) introgression of pummelo segments. They hypothe modern mandarins probably arose as hybrids of the existing sweet or
sized an explanation for this admixture pattern stating that an initial anges and mandarins (Fig. 1).
pummelo ancestor with parental haplotypes (P1/P2) first contributed to
the mandarin gene pool and with repeated backcrossing introgressed the
4
Grapefruit (C. paradisi Macf) hybridization product of lemon as the seed parent and sour orange as the
Grapefruit was believed to have originated more than 200 years ago pollen parent.
in the Caribbean region through hybridization of pummelo and sweet
orange (Barrett and Rhodes, 1976; Nicolosi et al., 2000). Molecular Rangpur lime (C. limonia Osbeck) and rough lemon (C. jambhiri Lush.)
marker studies based on InDel-SSRs (García-Lor et al., 2012), SNPs (Curk The lime term in ‘Rangpur’ lime was used by Swingle and Reece
et al., 2015) and haplotype allele share analysis (Curk et al., 2014) also (1967) for its slight similarity (small flowers and acidic nature) with
confirmed this hypothesis of pummelo x sweet orange for grapefruit and limes but Webber (1943) believed it had more resemblance with man
it was further supported by studies using whole genome sequencing (Wu darins and originated as cross product between lime and mandarin or
et al., 2014, 2018; Shimizu et al., 2016; Oueslati et al., 2017). Moreover, lime and sour (sunki) mandarin. Nicolosi et al. (2000), using RAPD
several hybrids later arose from cross events between oranges, modern markers, suggested that ‘Rangpur’ lime was a hybrid between citron and
admixed mandarins and grapefruits giving rise to tangors (a cross be mandarin; however, ‘Rangpur’ limes were also reported to be of man
tween mandarins and sweet oranges), tangelos (between grapefruit and darin genotype with few alleles introgressed by citron (Barrett and
mandarin) and orangelos (a hybrid of sweet orange and grapefruit) Rhodes, 1976). Later, Froelicher et al. (2011) reported mandarin as the
which are all collectively referred to as modern ‘small citrus’ breeding female contributor based on mitochondrial maternal phylogenetic
varieties (Oueslati et al., 2017). study. Further, principal component analysis (PCA) and structure anal
ysis by Curk et al. (2015) confirmed it as a direct hybridization product
Mexican lime (C. aurantiifolia (Christm.) Swingle) and Alemow (citron x mandarin) with equal contribution from both parents. Similar
(C. macrophylla Wester) reports have been observed (Barkley et al., 2006; Curk et al., 2016; Wu
Tanaka (1961) assigned two distinct names, C. aurantiifolia and et al., 2018; Ahmed et al., 2019), where Rangpur limes, khatta limes
C. macrophylla for ‘Mexican’ lime and alemow respectively, however, (C. karna) and rough lemons are direct hybridization products of citron
Swingle and Reece (1967) considered the two species as C. aurantiifolia. and mandarin.
Based on the parentage, Barrett and Rhodes (1976) suggested a trihybrid
origin (pummelo, citron and Microcitrus) for ‘Mexican’ lime, whereas Polyploid lime varieties
Nicolosi et al. (2000) proposed it to be a direct hybrid between citron It has been found that lime is the only naturally occurring Citrus
and papeda. The hypothesis of the latter was confirmed through popu species that includes polyploid germplasm besides having diploid
lation structure analysis by Curk et al. (2014), revealing an equal germplasm. For example, Curk et al. (2016) proposed that the allote
contribution of alleles from both citron and papeda. Similar dihybrid traploid ‘Giant key’ lime arose as a result of natural chromosomal
origin (citron x papeda) arising through independent reticulation events duplication event of ‘Mexican’ lime. This predominant disomic inheri
had also been reported for alemow and Adam’s apple (C. aurata Risso) tance of ‘Giant key’ lime was analyzed and confirmed through molecular
(Curk et al., 2015; Wu et al., 2018) with C. micrantha (papeda) as their marker studies (Rouiss et al., 2018) and substantiated through a GBS
maternal parent (Froelicher et al., 2011). study by Ahmed et al. (2019). Moreover, the origin of two important
triploid lime varieties, ‘Tahiti’ and ‘Tanepao’, resulted from interspecific
Lemon (C. limon (L.) Osbeck) hybridization between diploid gamete of ‘Mexican’ lime with lemon and
As suggested by Scora (1975) and Barrett and Rhodes (1976), lemons citron, respectively, revealing some more complex phylogenomic
originated as a direct hybrid between citron and lime, which later structures (Curk et al., 2016). Accordingly, all the four basic ancestral
revealed to be a natural hybrid of citron and sour orange based on taxa contributed to ‘Tahiti’ lime in which a haploid ovule of lemon
RAPD-RFLP (Nicolosi et al., 2000) and inter-simple sequence repeat [(mandarin x pummelo) x citron] fused with diploid pollen of ‘Mexican
(ISSR) (Gulsen and Roose, 2001) markers. Further, through InDel-SSR lime’ (citron x papeda) (Curk et al., 2016; Rouiss et al., 2018; Ahmed
marker analysis, three rare alleles in lemons were found to be shared et al., 2019, 2020). Additionally, the triploid lime ‘Tanepao’ originated
only with sour oranges that confirmed it as one of the parents for lemon from interploidy backcrosses between haploid pollen of citron and a
in addition to citron (García-Lor et al., 2012). Thus, lemons displayed a diploid ovule of ‘Mexican’ lime (citron x papeda) (Curk et al., 2016;
complex three-taxa structure resulting from interspecific hybridization Rouiss et al., 2018).
events between sour orange and citron (Curk et al., 2014, 2015). Thus, most modern citrus fruits are the interspecific cross among the
Recently, a genomic analysis by Wu et al. (2018) revealed lemons to four ancestral species, which has established the diversified phenotypic
have genomes from three species; mandarin (31 %), pummelo (18 %) characters. These characters eventually got fixed over time with vege
and citron (50 %). Also, identical chloroplast sequences between lemon tative propagation or apomixis.
and sour orange (pummelo x mandarin) confirmed it as a direct cross
between pollen of citron and an ovule of sour orange, which agreed with 4. Phylogeny of citrus and related genera
the previous studies of Ahmed et al. (2020); Carbonell-Caballero et al.
(2015) and Curk et al. (2016). The phylogenetic relationship of the genus Citrus with its close rel
atives (Fortunella, Poncirus, Microcitrus, Eremocitrus and Clymenia) seems
Bergamot (C. bergamia Risso) complicated due to compatible sexual relationships among them, which
Many hypotheses have been proposed for the origin of bergamot. is evidenced through different hybrid types viz. Citrange (Sweet orange
Some studies suggested it as a hybrid between sweet lime (C. limetta x P. trifoliata), Calamondin (Citrus x Fortunella), ‘Australian blood’ lime
Risso) and sour orange (Herrero et al., 1996a; Federici et al., 2000); few (Citrus x Microcitrus), Eremolemon (Citrus x Eremocitrus) etc., (Ollitrault
others proposed bergamot as a hybridization product between sour or et al., 2020). Moreover, phenomena such as mutations and poly
ange and citron (Nicolosi et al., 2000; Li et al., 2010). Based on haplo embryony add complexity to their taxonomic studies. Therefore, there
type share analysis, Curk et al. (2014) revealed the structure of has always been dispute regarding the placement of these related genera
bergamot to have heterozygous regions from both citron/pummelo and within Citrus or as separate genera. For example, Mabberley (1998) put
citron/mandarin. Later, admixture analysis by Penjor et al. (2016) forward the idea of incorporating the three related genera, Fortunella,
inferred the ratio of the three contributing genomes (pummelo, man Microcitrus and Eremocitrus, within the genus Citrus. This work was
darin and citron) to be 2:1:1 respectively. Moreover, nuclear and cyto supported by Bayer et al. (2009), where they also incorporated two more
plasmic marker (Curk et al., 2016) and parentage test (Shimizu et al., genera, i.e., Poncirus and Clymenia, within the genus Citrus, utilizing nine
2016) analyses suggested bergamot to be an offspring of sour orange and chloroplastic regions (trnL-F, rps16 spacer, atpB, rbcL-atpB spacer,
lemon. Recently, Ahmed et al. (2019) compared the karyotypes of trnDguc-psbM spacer, 5′ matK intron, trnS-trnG spacer, trnG intron,
bergamot with lemon and sour orange, confirming bergamot as a rps4-trnT spacer) for their phylogenetic studies. However, previously,
5
based on two chloroplast (cp) DNA regions, i.e. rps16 and trnL-trnF, groups with one being Poncirus and the other consisting of Citrus and
these related genera, namely Fortunella, Poncirus, Microcitrus, Eremoci related genera.
trus and Clymenia, were found sister to genus Citrus in the tribe Citreae
(Morton et al., 2003). Later, using three cpDNA fragments (trnL-trnF, Microcitrus and Eremocitrus
psbH-petB and trnS-trnG), Poncirus and Fortunella retained their position
as distinct clades and therefore, sister to Citrus, but Microcitrus, Eremo A close relationship between Microcitrus and Eremocitrus was estab
citrus and Clymenia were found to be nested with citron and papeda of lished in several studies (Barrett and Rhodes, 1976; Morton et al., 2003;
Citrus group (Lu et al., 2011). Recently, a study by Ghada et al. (2019), Abkenar et al., 2004; Penjor et al., 2010, 2013; Garcia-Lor et al., 2013)
using trnL intron region of cpDNA, showed separation of these related which could be attributed to their genetic resemblance as well as, their
genera from Citrus and hence, sister to genus Citrus except for Fortunella commonplace of origin. Morphologically, both the genera differed from
margarita (Citrus japonica var. margarita). Citrus in having dimorphic foliage and free stamens. Thus, both Micro
Although several studies on the phylogenetic relationship of Citrus citrus and Eremocitrus being endemic to Australia, were believed to have
with its related genera were done using specific nuclear DNA sequences originated years ago with a slower evolutionary rate that separated them
or partial chloroplastic sequences as markers (Bayer et al., 2009; Froe from the rest of Asian origin Citrus groups. However, both of these
licher et al., 2011; Penjor et al., 2013; Ramadugu et al., 2013; Amar Australian limes were reclassified into Citrus by Mabberley (1998) and at
et al., 2014), the lack of complete nuclear and chloroplastic genomes the same time, through RFLP markers, they were found to be nested
hindered their studies with stronger support. Therefore, to overcome within the papeda-pummelo cluster of Citrus (Federici et al., 1998),
this issue, a total of 34 chloroplast genomes from different Citrus species which was also observed in a study done by Uzun et al. (2009) using
were sequenced for the first time (Carbonell-Caballero et al., 2015), SRAP markers. Thereafter, using chloroplast genomes of thirty-four
which allowed comparing their maternal phylogeny and revealed these Citrus species, Carbonell-Caballero et al. (2015) demonstrated Micro
related genera (Fortunella, Poncirus, Microcitrus and Eremocitrus) to be citrus and Eremocitrus to be nested with Citrus medica (citron) cluster.
nested within Citrus group. Recently, a phylogenomic study through Further, chloroplastic SNP marker studies (Oueslati et al., 2016) and
whole-genome sequencing (WGS) by Wu et al. (2018) provided sub nuclear-genome studies (Wu et al., 2018) revealed a similar clustering of
stantial evidence for these related genera (Fortunella, Microcitrus and both Microcitrus and Eremocitrus with citrons where Wu et al. (2018)
Eremocitrus) to be included within the genus Citrus and Oueslati et al. provided a conclusive remark that the two Australian genera Microcitrus
(2016) put forth Clymenia to be considered within the genus Citrus, thus and Eremocitrus should be incorporated within the genus Citrus referring
making Citrus a monophyletic clade except for Poncirus, which was kept them as Australian Citrus species.
as a separate clade.
Clymenia
Fortunella
A small tree shrub, Clymenia was found to be the most distinguished
It was classified as a distinct genus because of its significant genus among all the related genera of Citrus and owing to its morpho
morphological differentiation from Citrus (Swingle and Reece, 1967). logical features i.e., differences in leaves, flowers and pulp vesicle’s
Several studies based on cpDNA (Nicolosi et al., 2000; Araujo et al., structure, it was considered most primitive genus of all the related
2003), amplified fragment length polymorphism (AFLP) (Pang et al., genera (Swingle and Reece, 1967; Spiegel-Roy and Goldschmidt, 1996).
2007), expressed sequence tag (EST)-SSR (Luro et al., 2008) were in However, molecular marker-based phylogenetic studies done by Bayer
support of this view of not placing Fortunella within Citrus. Contrast et al. (2009) and recently, by Oueslati et al. (2016), Clymenia was found
ingly, some phylogenetic studies based on DNA molecular markers and to be grouped with Australian limes (Microcitrus and Eremocitrus), which
barcodes suggested Fortunella to be nested within Citrus (Federici et al., were nested within the genus Citrus. Because of the inclusion of
1998; Barkley et al., 2006; Pang et al., 2007; Bayer et al., 2009; Uzun Australian limes as Citrus species, Clymenia was also suggested to be
et al., 2009; Penjor et al., 2010, 2013; Froelicher et al., 2011; Amar et al., incorporated within Citrus as a subgenus. However, the position of
2014). Later, a comprehensive whole-genome sequence (WGS) analysis Clymenia, among all the related genera of Citrus, remains unclear to date
by Wu et al. (2018) supported the nesting of genus Fortunella within that necessitates a deeper exploration of this genus and, with the
Citrus clade and suggested considering its species within the genus Cit availability of complete genomic information, is achievable.
rus, for example, Citrus japonica instead of Fortunella japonica.
5. Biogeographical origin of citrus and its dispersal
Poncirus
The origin of Citrus has always been a subject of controversy. How
Being deciduous with trifoliate leaves, Poncirus has a flowering ever, the wild genotypes of different Citrus species have been reported to
period and distribution patterns different from the rest of the Citrus be growing around Southeast Asian regions. For example, pummelo was
species and it was classified as a distinct genus from Citrus (Swingle and reported to grow in Indo-China, Malaysia, Yunnan and Hainan (Scora,
Reece, 1967). With the advent of molecular markers, a study using RFLP 1988; Gmitter and Hu, 1990). Mandarin diversification occurred
and RAPD (Federici et al., 1998) revealed Poncirus to be nested within a through a large area covering north-eastern India, southern to southeast
subclade consisting of lime and papeda of the Citrus group. This was China (Hodgson, 1967; Swingle and Reece, 1967). Citron evolved in
further substantiated by some of the studies, including both chloro northeastern, southern and central India, Bhutan, Myanmar,
plastic and DNA based molecular markers that reported Poncirus to be Bangladesh, and Yunnan (Tanaka, 1961; Gmitter and Hu, 1990) while
nested within the Citrus group (Araujo et al., 2003; Luro et al., 2008; papeda originated in the Philippines (Zhou, 1991). Also, the wild hy
Bayer et al., 2009; Uzun et al., 2009; Penjor et al., 2010, 2013; Amar brids of Citrus are predominant in areas of their parental genotypes.
et al., 2014; Carbonell-Caballero et al., 2015). However, contradictions Accordingly, ‘Rangpur’ lime, a hybrid of mandarin and citron, appears
were observed in some molecular marker studies using PCR-RFLP around eastern Guangxi and mostly in southern Tibet (Gmitter and Hu,
(Abkenar et al., 2004), SSR (Barkley et al., 2006), AFLP (Pang et al., 1990) while, rough lemon, another cross between mandarin and citron,
2007), cpDNA (Lu et al., 2011) that reported Poncirus to be sister to is reported in India (Hodgson, 1967). A hybrid of Fortunella and man
genus Citrus and formed a monophyletic lineage. Recently, a study darin, known as Calamondin, is widely cultivated in the Philippines and
conducted by Wu et al. (2018) based on whole nuclear genome phylo China. Therefore, many propositions regarding the biogeographical
genomics and using single nucleotide polymorphic (SNP) markers origin of Citrus species have been made for a long time, and one of the
concluded Poncirus to be a distinct clade, resulting in two monophyletic pioneer visions given by Vavilov (1935) assumed the Indo-Burma center
6
(Assam and Burma) and the Indo-Malayan center as the two centers of west (Wu et al., 2018).
origin for Citrus whereas Tolkowsky (1938) suggested the center of As citrus domestication started to happen in the southeast Asian
origin to be in the north-east Indian region and somewhere in the origin, specifically in China and India, thereafter, the spread of Citrus
mountainous parts of southern China. Later, Tanaka (1954) assumed a species began to take place throughout the rest of the world. It has been
boundary line and proposed it to run from the border of north-west India reported that Alexander the Great introduced citrons in the Mediterra
to China’s Yunnan province by covering Burma and finally reaching nean basin from India for the first time around 300 BC, and later, other
south of the island of Hainan, but Gmitter and Hu (1990) were rather Citrus species started to spread from southeast Asia to Europe and North
more precise to recognize the Yunnan province of China as the central Africa through the Mediterranean region. For example, sour orange and
origin region due to the presence of wide diversity of Citrus species. lemon reached the Mediterranean basin around the 10th century, while
While all these studies revealed Asia, specifically southeast Asia, to pummelo and lime around the 13th century and sweet orange around
be the center of origin for Citrus, few also suggested Australia and its the 15th century (Ollitrault and Navarro, 2012). However, it was also
nearby parts to be the origin (Swingle and Reece, 1967; Scora, 1988). found that until the onset of the 19th century, mandarins did not arrive
However, all the conflicts of Australian origin were overruled through in Europe. The introduction of Citrus species in America occurred around
molecular dating and whole-genome phylogenetic analysis which the 15th century by Christopher Columbus, who took seeds of oranges,
established that the Citrus species went through a rapid Asian radiation citrons and lemons on his second trip to Hispaniola island in 1483.
in the late Miocene period (6–8 Million years ago, Mya). After that, Around the 16th century, Spanish explorers spread citrus from Central
Australian radiation was witnessed in the early Pliocene epoch, i.e., America to Florida while the Portuguese introduced it in Brazil (Fig. 2).
around 4 Mya, suggesting that migration of the ancestral Citrus species Further, the seeds of limes, lemons and oranges were taken from Brazil
might have occurred through the Wallace line, which earlier used to be to Australia around the 18th century by different colonists (Ollitrault
the barrier for dispersal of different species (Wu et al., 2018). Hence, the and Navarro, 2012).
study concluded that the spread of Citrus species started from southeast
Asia. By considering the regions of Yunnan province of southwest China, 6. Genetic basis of modern citrus domestication
Myanmar and Northeast India to be centers of origin and later, possibly
through transoceanic dispersals, these species migrated to Australia and Citrus fruits, especially the commercially important varieties such as
adapted to its diverse climates, thus, rejecting the idea of primary cen sweet and sour oranges, mandarins, lemons, limes and grapefruits
ters being located in Australia or nearby islands. Evidence on similar cultivation, gained immense popularity worldwide but unfortunately
kinds of relocation by other migrating angiosperms from Southeast Asia with an unclear history of evolution and domestication. Hence, the
has also been found (Thomas et al., 2012), which coincided with the following section details some of the crucial aspects of citrus domesti
extensive monsoon weakening and heavy seasonal rains. Due to these cation: apomixis, self-incompatibility, palatability, pigmentation and
factors, today’s Citrus species are considered mesophytes with xero fruit size that evolved from the wild to cultivated varieties for human
phytic adaptations like waxy leaves and fruit peel, individual juice sacs consumption. The use of words ‘mandarin’ and ‘pummelo’ in this section
and low photosynthesis and transpiration rates. Thus, after the late refers to the cultivated ones, while ‘wild mandarin’ refers to the ancient
Miocene-species radiation event, Citrus species started to diverse mostly ones without introgression.
from west to east directions of the assumed center of origin, i.e., towards
the east (Fortunella and mandarins), north-east (papedas) and southeast
(pummelos and papedas) except for citrons that migrated towards the
Fig. 2. Origin and dispersal of Citrus species around the world.

(C indicates century, BC: Before Christ). Adapted from Ollitrault and Navarro (2012) and Wu et al. (2018).
7
6.1. Apomixis 6.2. Self-incompatibility (SI)
Citrus, like many other fruit crops, can propagate naturally through Unlike apomixis that fixes genetic variability, citrus exhibits another
asexual means apart from sexual reproduction. One such mode is special reproductive feature of self-incompatibility (SI) that promotes
nucellar embryony or apomixis, where many somatic embryos develop outcrossing and hence, genetic diversity. Many angiospermic plants
directly from nucellar or integument cells with or without its zygotic utilize this important mechanism of SI when self-fertilization is pre
embryo (polyembryony) (Koltunow et al., 1996; Zhang et al., 2018). As vented by the rejection of pollen from the same genotype and accepting
a result, the offsprings produced by apomixis are identical to its non-self pollen (Nettancourt, 2001). The SI is mainly controlled by a
maternal genotype and this heritable trait (apomixis) in citrus has single co-dominant multi-allelic locus termed as S-locus encoding two
gained considerable attention by agriculturists to generate massive tightly linked specificity (S) determinants/ genes for both male (pollen)
proportions of genetically uniform rootstocks despite its genome having and female (pistil) segregated together in a unit as (S) haplotypes
a high level of heterozygosity (Woo et al., 2019). Data from various (Takayama and Isogai, 2005). The SI response operates when the same S
germplasm resources have identified most commercial citrus varieties haplotypes deploy the S determinants to initiate a protein-protein
(mandarins, oranges, lemons, grapefruits) and the two sexually interaction for differentiating self/non-self. Depending upon the gene
compatible genera of Citrus viz. Fortunella (except F. margarita and F. action on pollen’s SI phenotype, SI can be classified into two categories-
japonica) and Poncirus to be polyembryonic (Kepiro and Roose, 2009; sporophytic SI (SSI) when, the pollen’s S phenotype is determined by
Zhang et al., 2018). Several genetic studies were done to understand the S-genotype of the diploid genome of its sporophytic parents while in
evolution and mechanism of polyembryony in Citrus and related genera. gametophytic SI (GSI), it is determined by individual haploid micro
Based on ratios of segregating populations, it has been shown either a spores (Nettancourt, 2001). Plants belonging to Brassicaceae exhibit SSI,
single dominant gene (Parlevliet and Cameron, 1959) or more than one while members of Solanaceae, Rosaceae, Scrophulariaceae etc., exhibit
gene (Iwamasa, 1967; Cameron and Soost, 1979; Hong et al., 2001) to be GSI (Newbigin et al., 1993). However, several studies have shown citrus
responsible for controlling polyembryony. Later, molecular to exhibit Solanaceae-type of GSI, which in turn is responsible for
marker-based studies identified genes linked to polyembryony in both seedless fruit production in many cultivable varieties like ‘Wuzisha
Citrus and Poncirus species (Kepiro and Roose, 2009; Raga et al., 2012) tangju’ mandarin (Ye et al., 2009), ‘Xiangshui’ lemon (Zhang et al.,
and the locus for polyembryony was after that mapped on a genomic 2012), ‘Afourer’ mandarin (Gambetta et al., 2013), ‘Kagzi kalan’ lemon
region spanning approximately 380 kb with 70 open reading frames (Kakade et al., 2017) etc. The demand for more seedless varieties rather
(ORFs) and sequenced (Nakano et al., 2008a, 2008b, 2012). Further, to than seeded ones is preferred in the markets, as the highly seeded fruits
gain a deeper insight on citrus polyembryony, transcription-based ap delimit the quality and further commercial values of fruits (Gambetta
proaches were used to identify differentially expressed genes in poly- et al., 2013). Thus, in the absence of cross fertilization, many citrus
and mono-embryonic cultivars (Nakano et al., 2013; Kumar et al., 2014; cultivars can produce seedless fruits asexually through parthenocarpy.
Long et al., 2016), along with a more comprehensive multi-omics Therefore, SI is an important commercial trait in citrus breeding as its
approach (Wang et al., 2017) which screened the genetic locus combination with parthenocarpy significantly reduces seed production
responsible for polyembryony in citrus. Hence, the earlier reported 380 otherwise produced by sexual reproduction. Hence, studies to determine
kb genomic region (Nakano et al., 2012) was cut short to an 80-kb region S-haplotypes and S-allele frequencies in citrus became vital to decipher
harboring eleven potential genes, of which the gene CitRWP, was highly the genes involved in SI and, consequently, the molecular mechanism
expressed in ovules of polyembryonic rather than monoembryonic citrus involved. Thus, a study performing 52 crosses with different citrus
cultivars. In fact, the role of this CitRWP gene having an RWP-RK domain cultivars to evaluate the distorted segregation of an isoenzyme linked to
analogous to the RKD protein family of Arabidopsis species was earlier S gene, revealed a total of 8 alleles (S1-S8) for the S gene (Ngo et al.,
demonstrated to serve as regulatory genes associated with the egg cell 2011). Further, the alleles S9S10 (Kim et al., 2010), S1S2 (Kim et al.,
and pattern formation in the embryo (Kőszegi et al., 2011; Waki et al., 2011), S4S5 (Zhou et al., 2018) and S3S11 (Kim et al., 2020) were sub
2011; Koi et al., 2016). Moreover, the study by Wang et al. (2017) on sequently identified in later studies.
expressional changes also revealed an insertion of a transposable With the onset of next-generation sequencing (NGS) technologies,
element- MITE (miniature inverted-repeat transposable element) in the RNA-Seq and comparative transcriptomics accelerated the identification
CitRWP gene promoter region that co-segregated with all the poly of genes contributing to SI in citrus (Caruso et al., 2012; Zhang et al.,
embryonic cultivars supporting the role of the candidate gene CitRWP 2014; Ma et al., 2017) but with no direct evidence of those genes to be
controlling polyembryony in citrus. Another study also identified the the S-determinants for gametophytic self-incompatible Citrus species. In
gene CitRKD1 from the polyembryonic locus of citrus to be a potential general, the female S determinant in GSI is a gene encoding glycoprotein
candidate for somatic embryogenesis (Shimada et al., 2018). Interest with ribonuclease activity (S-RNase) expressed exclusively in the upper
ingly, the study revealed the presence of CitRKD1 gene in the repro segment of style to degrade the RNA of incompatible pollen (McClure
ductive tissues of most polyembryonic citrus cultivars containing et al., 1989; Takayama and Isogai, 2005). Whereas multiple genes
multiple alleles with two main categories- polyembryonic alleles (with encoding for S-locus F- box (SLF) proteins involved in the ubiquitin
MITE insertion) and monoembryonic alleles (without MITE insertion). pathway serve as the male S-determinant expressed exclusively in the
Moreover, failure to induce somatic embryogenesis due to loss of func pollen (Kubo et al., 2010; Williams et al., 2014). As data from numerous
tional CitRKD1 in transgenic sweet orange also evidenced the role of citrus accessions revealed many S-RNase homologues, hypotheses
CitRKD1 to be essential for polyembryony, especially with a MITE regarding S-RNase based SI system have been made for citrus (Chai
insertion as an effective upstream regulator. However, the role of the et al., 2011; Miao et al., 2011; Zhang et al., 2014; Liang et al., 2017).
genes (CitRWP and CitRKD1) associated with MITE insertion is yet to be Eventually, this S-RNase based SI system was proved by Liang et al.
explored in Poncirus and Fortunella for a better understanding of the (2020), who evidenced the presence of an S-locus in pummelo, carrying
mechanism that triggers polyembryony in these species. Thus, based on S-RNases and several SLFs. This study was consistent with other
the following studies on citrus polyembryony, it can be suggested that S-RNase-SLFs-based non-self recognition models and further confirmed
the trait of apomixis was purposefully chosen during the course of citrus through in-vitro bioassay demonstrating the inhibition of pollen tube
breeding programs due to its ability to fix valuable characters which is growth. They showed each of those S-RNases to be linked to almost nine
also underpinned by the occurrence of this trait in most cultivable citrus SLFs and their highly polymorphic sequence analysis revealed them to
varieties. be co-evolved. However, another interesting outcome was revealed from
the same study where they came across a shortened sequence of S-RNase
in C. sinensis with one nucleotide deletion at 443rd position causing
8
frame shift mutation (termed as Sm-RNase) with a premature stop codon found it to be highly divergent in the cultivated and wild mandarins.
that occurred in all self-compatible (SC) citrus accessions. Upon analysis Based on the genomic and transcriptomic data, they evidenced the se
of citrus population for Sm-RNase, they suggested Sm-RNase in SC citrus lection of ACO alleles during the domestication of mandarins and
accessions first arose in wild mandarins that further transferred to observed it to be downregulated in the wild mandarins.
cultivated mandarins and its hybrids and eventually got fixed over time Besides the sweet/sour taste, the evolution of ‘bitterness’ (in
possibly through apomixis and selfing. pummelo, grapefruit, bitter orange) to ‘non-bitterness’ (in mandarin,
sweet orange, lime) is another aspect of palatability under citrus
6.3. Palatability domestication. Branched-chained glycosides (flavanone), the predomi
nant flavonoids in citrus was reported to be the primary cause for
Apart from modification of the reproductive machinery, one of the bitterness, with neohespirosides (naringin and neohesperidin) and
key features leading to domestication is palatability. As far as citrus is rutinosides (narirutin and hesperidin) being the contributing flavanones
concerned, sweetness, sourness and bitterness (in some cases) are the relating to bitterness and non-bitterness in Citrus species, respectively
common flavors responsible for attracting human tastes for cultivation (Peterson et al., 2006a, 2006b). The enzyme rhamnosyltransferase
and governing the commercial market. Acidity is one of the important (Rhat) catalyzes branched-chain rhamnosylation of flavanone-7-O-glu
traits for citrus breeders that is mainly regulated by the pH of juice cose to form either neohespirosides (by enzyme 1,2-Rhat) or rutinosides
vesicle cell vacuoles. The variation in acidity gives rise to two major (by 1,6-Rhat) and the genes encoding these enzymes have been char
palatable variants- ‘sweet’ (less acidic/non-sour) and ‘sour’ (more acterized in pummelo (Citm1,2-Rhat, here m denotes C. maxima) for
acidic) in different citrus varieties. It has been deduced that a proton neohespiroside production and in sweet orange (Cits1,6-Rhat, s refers to
gradient in vacuolar membrane triggers a massive influx of citric acid in C. sinensis) for rutinoside production (Frydman et al., 2004, 2013). The
its dissociated form, thereby increasing its buffering capacity and phylogenetic analysis of the two genes revealed them to be distantly
imparting acidic (sour) taste (Brune et al., 1998, 2002; Shimada et al., related, although, both had originated individually before citrus speci
2006; Neta et al., 2007). Afterwards, the role of two citrus PH homologs ation suggesting the gene Citm1,2-Rhat to be correlated for positive se
(CitPH1 and CitPH5), encoding for vacuolar P-ATPases proton pump (Li lection which perhaps, imparted bitterness in pummelo, while the gene
et al., 2016), responsible for sour taste in citrus was investigated. It was Cits1,6-Rhat was responsible for sweetness in mandarin and orange
found that the expression levels of both (CitPH1 and CitPH5) signifi (Frydman et al., 2013). Further, the presence of an ortholog Citm1,2Rhat
cantly altered in different citrus varieties; while it was upregulated in was evidenced in sweet oranges, which was totally absent in mandarin,
acidic ones (pummelo, sour orange, sour lemon, rangpur lime) but indicating sweet oranges might have accumulated it from pummelo
drastically downregulated in non-acidic (sweet) ones (Strazzer et al., (being its maternal contributor) and later, possibly through frameshift
2019). The same study also revealed an inactivating mutation of tran mutation, might have evolved as a non-bitter tasting fruit (Frydman
scription factor CitAN1 required for the expression of CitPH1 and CitPH5 et al., 2013). Recently, three 1,2Rhat homolog genes coding for di-glu
that reduced the acidity in sweet lime and sweet oranges with additional cosyltransferases (CitdGlcTs) that transfer glucose to
regulatory mutations of other transcription factors (CitPH3 and CitPH4) flavanone-7-o-glucose (F7G) to form F7GG, imparting non-bitter taste,
acting on multiple genes suggesting a reduced acidity in many citrus was revealed in various Citrus genomes (Chen et al., 2019). This infor
varieties at different stages of domestication. Thus, it is apparent that the mation provides a future scope to improve the flavor for human con
reduction in acidity had been a desirable choice for human palatability, sumption by transgenic approaches of knocking out Cit1,2Rhat and
which was reflected as a positive selection during cultivation. This can enhancing CitdGlcTs expression in pummelo fruits.
be supported by the work of Wu et al. (2018), who conducted a
genome-wide association study (GWAS), taking thirty-seven citrus ac 6.4. Pigmentation and fruit size
cessions with their known acidity and located a nearly 2 Mb locus at the
beginning of chromosome 8 (0.3–2.2 Mb) as potential candidate loci As colors are one of the striking visual features, the contribution of
associated with palatability, revealing all the palatable mandarins (with flavonoids in pigmentation apart from palatability is also remarkable
reduced acidity) showed pummelo admixture in that locus. However, during citrus domestication leading to characteristic color patterns
the acidic ones were devoid of any pummelo admixture indicating the varying from those of wild varieties. Flavonoids, especially anthocya
possibility of introgressing pummelo genes involved in mandarin nins, impart colors to flowers, seeds, fruits and other plant tissues. In
domestication. This chromosomal region harbored fifteen discrimina angiosperms, anthocyanin biosynthesis seemed to be controlled by three
tory SNPs and several potential genes related to acidity regulation in conserved complexes (MYB/bHLH/WD40, MBW) resulted from the
citrus. Among these, a gene (Ciclev10028714) coding for mitochondrial interaction of transcription factors- MYB, basic helix-loop- helix (bHLH)
NAD + isocitrate dehydrogenase (NAD + IDH) was involved in the and WD40-repeat proteins (Xu et al., 2015). Anthocyanin production in
catalytic conversion of isocitrate to α-ketoglutarate, an important reac citrus is activated by a transcriptional factor, Ruby, which is a regulatory
tion step for citric acid synthesis in Krebs cycle (Meléndez-Hevia et al., MYB gene (Butelli et al., 2012). On investigating several different Ruby
1996). To further understand the genetic basis of mandarin selection, alleles (Butelli et al., 2017), a difference in the pigmentation pattern was
domestication and its relation to pummelo introgression, Wang et al. observed, resulting in a range of phenotypes from pigmentation sup
(2017) conducted a study by collecting both cultivable and wild man pression to new pigment formation. This variation was mainly due to the
darins from regions of China that harbor several indigenous mandarin transposable elements that might have been inserted or deleted to
cultivars. They revealed that the citric acid levels between the cultivated change the activity of Ruby gene, thereby affecting the color of petals.
and wild mandarins significantly differed, keeping their sugar level Hence, this factor was probably one of the reasons that the Chinese
almost the same. On searching for candidate regions for domestication tradition positively selected the white flowers in mandarins and oranges
in genomes of mandarin varieties and identifying the genes associated as it symbolizes purity and innocence.
with citric acid biosynthesis and regulation, the study revealed dissim Moreover, such mutations have been fascinating for plant breeders
ilarities at the region of a gene DLAT1 (Cs7g_pb021730) encoding py and scientists for a long time as an interesting phenomenon of acidity in
ruvate dehydrogenase complex between wild and cultivable mandarins. limes and lemons was directly associated with anthocyanin pigmenta
As acidity was drastically decreased during the domestication of wild tion (Chapot, 1950; Hodgson, 1967). Apparently, the wild citrus vari
mandarins, reduction of citric acid, especially by pyruvate substrate, eties were found to have colored flowers and acidic nature. In contrast,
was considered a marker trait for mandarin domestication. The same the cultivable varieties with white flowers and seeds were less acidic or
study also identified another gene encoding an isoform of aconitate rather “sweet” in taste. This genetic link of pigmentation with fruit
hydratase (ACO) which controlled the citrate content of ripe fruit, and acidity was recently investigated by Butelli et al. (2019), who identified
9
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Perspectives in Plant Ecology, Evolution and Systematics 53 (2021) 125644

Contents lists available at ScienceDirect

Perspectives in Plant Ecology, Evolution and Systematics

A molecular perspective on the taxonomy and journey of

Fig. 1. Genealogy of cultivable Citrus species.

Fig. 2. Origin and dispersal of Citrus species around the world.

6.1. Apomixis 6.2. Self-incompatibility (SI)

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