Skip to main content
eScholarship
Open Access Publications from the University of California

Complex history of admixture during citrus domestication revealed by genome analysis

  • Author(s): Wu, G. Albert
  • Prochnik, Simon
  • Jenkins, Jerry
  • Salse, Jerome
  • Hellsten, Uffe
  • Murat, Florent
  • Perrier, Xavier
  • Ruiz, Manuel
  • Scalabrin, Simone
  • Terol, Javier
  • Takita, Marco Aurélio
  • Labadie, Karine
  • Poulain, Julie
  • Couloux, Arnaud
  • Jabbari, Kamel
  • Cattonaro, Federica
  • Fabbro, Cristian Del
  • Pinosio, Sara
  • Zuccolo, Andrea
  • Chapman, Jarrod
  • Grimwood, Jane
  • Tadeo, Francisco
  • Estornell, Leandro H.
  • Mu?oz-Sanz, Juan V.
  • Ibanez, Victoria
  • Herrero-Ortega, Amparo
  • Aleza, Pablo
  • Pérez, Julián Pérez
  • Ramon, Daniel
  • Brunel, Dominique
  • Luro, Francois
  • Chen, Chunxian
  • Farmerie, William G.
  • Desany, Brian
  • Kodira, Chinnappa
  • Mohiuddin, Mohammed
  • Harkins, Tim
  • Fredrikson, Karin
  • Burns, Paul
  • Lomsadze, Alexandre
  • Borodovsky, Mark
  • Reforgiato, Giuseppe
  • Freitas-Astua, Juliana
  • Quetier, Francis
  • Navarro, Luis
  • Roose, Mikeal
  • Wincker, Patrick
  • Schmutz, Jeremy
  • Morgante, Michele
  • Machado, Marcos Antonio
  • Talon, Manuel
  • Jaillon, Olivier
  • Ollitrault, Patrick
  • Gmitter, Frederick
  • Rokhsar, Daniel
  • et al.
Abstract

Although Citrus is the most globally significant tree fruit, its domestication history is poorlyunderstood. Cultivated citrus types are believed to comprise selections from and/or hybrids of several wild progenitor species, but the identities of these progenitors, and their contribution to modern cultivars, remain controversial. Here we report the genomes of a collection of mandarins, pummelos, and oranges, including a high quality reference sequence from a haploid Clementine mandarin. By comparative genome analysis we show that these cultivated types can be derived from two progenitor species. Cultivated pummelos represent selections from a single progenitor species C. maxima. Unexpectedly, however, we find that cultivated mandarins are introgressions of C. maxima into a distinct second population that we identify with the ancestral wild mandarin species C. reticulata. Sweet and sour oranges are found to be interspecific hybrids. Sweet orange, the most widely cultivated citrus, arose as the offspring of previously admixed individuals. In contrast, sour (or Seville) orange is an F1 hybrid of pure C. maxima and C. reticulata parents, implying that wild mandarins were part of the early breeding germplasm.Surprisingly, we also find that a wild Chinese mandarin from Mangshan, China showssubstantial sequence divergence from C. reticulata and appears to represent a distinct taxon.Understanding the relationships and phylogeny of cultivated citrus through genome analysis will clarify taxonomic relationships and enable previously inconceivable opportunities for sequence-directed genetic improvement.Citrus are widely consumed worldwide as juice or fresh fruit, providing important sources ofvitamin C and other health-promoting compounds. Global production in 2012 exceeded 86million metric tons, with an estimated value of US$9 billion (http://www.fas.usda.gov/psdonline/circulars/citrus.pdf). The very narrow genetic diversity of cultivated citrus makes it highly vulnerable to disease outbreaks, including citrus greening disease (also known as Huanglongbing) that is rapidly spreading throughout the world's major citrus producing regions1. Understanding the population genomics and domestication of citrus will enable strategies for improvements to citrus including resistance to greening and otherdiseases. The domestication and distribution of edible citrus types began several thousand years ago in Southeast Asia and spread globally following ancient land and sea routes. The lineages that gave rise to most modern cultivated varieties, however, are lost in undocumented antiquity, and their identities remain controversial2, 3. Several features of Citrus biology and cultivation make deciphering these origins difficult. Cultivated varieties are typically propagated clonally by grafting and through asexual seed production (apomixis via nucellar polyembryony) to maintain desirable combinations of traits (Fig. 1). Thus many important cultivar groups have characteristic basic genotypes that presumably arose through interspecific hybridization and/or successive introgressive hybridizations of wild ancestral species. These domestication events predated the global expansion of citrus cultivation by hundreds or perhaps thousands of years, with no record of the domestication process. Diversity within such groups arises through accumulated somatic mutations, generally without sexual recombination, either as limb sports on trees or variants among apomictic seedling progeny.Two wild species are believed to have contributed to domesticated pummelos, mandarins and oranges. Based on morphology and genetic markers, pummelos have generally been identified with the wild species C. maxima (Burm.) Merrill that is indigenous to Southeast Asia. Although mandarins are similarly widely identified with the species C. reticulata Blanco 4-6, wild populations of C. reticulata have not been definitively described. Various authors have taken dif

Main Content
Current View