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Diversité des fruits d'agrumes © Patrick Ollitrault

A new look at the evolution of Citrus

An international study involving CIRAD and INRA, published in the journal Nature on 7 February 2018, has revolutionized the botanical classifications of citrus fruits. The work revealed ten true Citrus species, four of which are behind modern cultivated varieties such as oranges, mandarins, grapefruits, pummelos, citrons, lemons and limes. This information paves the way for new varietal breeding strategies for these fruits, which are amongst the most widely grown worldwide.

Updated on 02/21/2018
Published on 02/08/2018

Following on from work by the International Citrus Genomics Consortium,which produced the Citrus reference genetic sequence in 2014 (1), scientific teams from Spain, the USA and France (CIRAD and INRA) joined forces to analyse the evolution of the genus Citrus and related genera (2). Based on complete genome data for 60 varieties and wild forms representative of the diversity of Citrus, the scientists came up with a new evolutionary model for the genus Citrus. The model calls into question the taxonomic systems developed for Citrus in the 1960s, which continues to account for the existence of three different botanical classifications for Citrus.
  

Two phases of spread cast doubt on the borders of the genus Citrus

The phylogenomics work done within this study revealed ten true species amongst the 60 varieties analysed. Those ten species are the result of some eight million years of evolution, during which scientists now recognize two major phases of evolutionary diversification: the first in Asia at the end of the Miocene period, between six and eight million years ago, and the second in Australia at the start of the Pliocene period, around four million years ago. The first phase may be linked to a dramatic reduction in monsoons in Asia at the time, and led to a separation into eight branches, including four ancestral species from which cultivatedCitrusvarieties originated. The second phase resulted in three Australian lime species.

Origine supposée des agrumes et voies de dispersion historique. © INRA, Franck Curk
© INRA, Franck Curk

  

The main modern Citrus groups trace their origins to four ancestral species

Four of those ten true species, C. reticulata, C. maxima, C. medica and C. micrantha, correspond to four modern Citrus groups, respectively: mandarins, pummelos, citrons and a papeda known as biasong in the southern Philippines, where it originated. Through natural interspecific hybridization, these four ancestral species subsequently resulted in most cultivated varieties, including oranges, grapefruits, lemons and limes.

  

L'origine des agrumes cultuvés revisitée : quelques exemples en images. © INRA & CIRAD, Franck Curk et Patrick Ollitrault
© INRA & CIRAD, Franck Curk et Patrick Ollitrault

 

Certain groups, such as sour oranges, rough lemons and Rangpur limes or Mexican limes are the result of direct hybridization between these four ancestral species, respectively: C. maxima x C. reticulata, C. micrantha x C. medica. Others, such as lemons, sweet oranges and grapefruits, resulted from more complex evolutions, involving interspecific recombination. "Lemon, for instance, is a hybrid between a sour orange and a citron; grapefruit a hybrid between a pummelo and a sweet orange", Franck Curk from INRA explains. "Sweet oranges, for their part, have a complex structure resulting from a mixture of two ancestral species, C. reticulata and C. maxima. Their exact origin is not yet clear", Patrick Ollitrault from CIRAD adds.

"Unlike modern citrons and pummelos, which appear to be pure representatives of the species C. medica and C. maxima, all cultivated mandarins have parts of their genome drawn from pummelos. This natural introgression may have played a major role in the domestication of mandarins, in particular by modifying the synthesis of certain acids, making their fruits more popular",Franck Curk points out.
  

Towards more innovative varietal breeding strategies

In addition to identifying the ancestral species that gave rise to cultivated Citrus varieties, the study served to pinpoint the origin, throughout the genome, of the different Citrus chromosome fragments. These complex structures largely govern the essential traits that determine the typicality of an orange, a grapefruit, a lemon or a lime. Where as conventional breeding (through sexual crossing) of these cultivated varieties previously looked to be impossible, detailed knowledge of ancestral species and their structures paves the way for innovative breeding strategies."This knowledge enables us to target the parents of future varieties more efficiently. When crossing, the aim is to rebuild these structures using the diversity of the ancestral species or of intermediate horticultural groups. This type of strategy is already being developed by CIRAD and INRA with a view to diversifying limes in Corsica and Guadeloupe", Patrick Ollitrault reveals.

 

A "Citrus" Biological Resource Centre in Corsica, to support research and development

INRA and CIRAD have access to one of the four largest Citrus collections for their research. The Biological Resource Centre in question, at San Giuliano in Corsica, covers 14 ha and comprises more than 1100 cultivated varieties from some 50 countries. It is the world's most diverse mandarin collection, and is a valuable tool for research ranging from genomics to participatory breeding of new Citrus varieties with stakeholders in Mediterranean and tropical supply chains. Those new varieties must satisfy market demand and respond to the constraints faced by the supply chains, such as new diseases (for instance Huanglongbing) or pests, and increasing drought and soil salinization because of climate change. The research conducted has local, regional, national and global impacts, since Citrus production is one of the major fruit sectors worldwide, with 125 million tonnes produced each year on the five continents.

Contact(s)
Scientific contact(s):

Press Relations:
Inra News Office (+33 (0)1 42 75 91 86), Sophie Della Mussia / presse Cirad (+33 (0)7 88 46 82 85)
Associated Division(s):
Plant Biology and Breeding
Associated Centre(s):
Corsica

Référence

Guohong Albert Wu, Javier Terol, Victoria Ibanez, Antonio López-García, Estela Pérez-Román, Carles Borredá, Concha Domingo, Francisco R. Tadeo, Jose Carbonell-Caballero, Roberto Alonso, Franck Curk, Dongliang Du, Patrick Ollitrault, Mikeal L. Roose, Joaquin Dopazo J, Frederick G. Gmitter Jr.Daniel S. Rokhsar and Manuel Talon. 2018. Genomics and phylogenetic analyses of Citrus origins and evolution. Nature. On line First DOI:10.1038/nature25447

http://www.nature.com/nature

Partenaires

Centro de Genómica, Instituto Valenciano de Investigaciones Agrarias, Espagne

US Department of Energy Joint Genome Institute, USA.

Computational Genomics Department, Centro de Investigación Príncipe Felipe (CIPF), Espagne

Unité Mixte de Recherche Amélioration Génétique et Adaptation des Plantes (UMR Agap), Cirad, Inra, France

Department of Botany and Plant Sciences, University of California, Riverside, USA.

Functional Genomics Node, Spanish National Institute of Bioinformatics, (ELIXIR-es) at CIPF, Espagne

Citrus Research and Education Center (CREC), Institute of Food and Agricultural Sciences (IFAS), University of Florida, Lake Alfred, USA

University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, USA.         

 

Autres références bibliographiques

Origin of C. latifolia and C. aurantiifolia triploid limes: The preferential disomic inheritance of doubled-diploid 'Mexican' lime is consistent with an interploid hybridization hypothesis. Rouiss Houssem, Bakry Frédéric, Froelicher Yann, Navarro Luis, Aleza Pablo, Ollitrault Patrick. 2017. Annals of Botany, 15 p.

https://doi.org/10.1093/aob/mcx179

Genotyping by sequencing reveals the interspecific C. maxima / C. reticulata admixture along the genomes of modern citrus varieties of mandarins, tangors, tangelos, orangelos and grapefruits. Oueslati Amel, Salhi-Hannachi Amel, Luro François, Vignes Hélène, Mournet Pierre, Ollitrault Patrick. 2017. PloS One, 12 (10), e0185618 (22 p.)

http://dx.doi.org/10.1371/journal.pone.0185618

Phylogenetic origin of limes and lemons revealed by cytoplasmic and nuclear markers.  Curk Franck, Ollitrault Frédérique, Garcia-Lor Andrés, Luro François, Navarro Luis, Ollitrault Patrick.  2016.    Annals of Botany, 117 (4): 565-583.

http://dx.doi.org/10.1093/aob/mcw005

Nuclear species-diagnostic SNP markers mined from 454 amplicon sequencing reveal admixture genomic structure of modern Citrus varieties.  Curk Franck, Ancillo Gema, Ollitrault Frédérique, Perrier Xavier, Jacquemoud-Collet Jean-Pierre, Garcia-Lor Andrés, Navarro Luis, Ollitrault Patrick.  2015.    PloS One, 10 (5), e0125628 (25 p.) 

http://dx.doi.org/10.1371/journal.pone.0125628