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Citrus Genomics, Phylogenetics Traces Fruits' Origins

NEW YORK (GenomeWeb) – A genomic analysis of some 60 citrus accessions has upended previously proposed taxonomic classifications.

Researchers led by the US Department of Energy's Joint Genome Institute's Guohong Albert Wu sequenced 30 citrus fruit genomes and compared them to previously sequenced genomes to unravel the genealogy and evolutionary history of citrus. As they reported in Nature today, they traced the origin of citrus to the Himalayan foothills during the late Miocene and also found that some genera previously thought to be distinct actually fall within the citrus clade.

"[T]his work presents insights into the origin, evolution and domestication of citrus, and the genealogy of the most important wild and cultivated varieties," Wu and his colleagues wrote in their paper. "Taken together, these findings draw a new evolutionary framework for these fruit crops, a scenario that challenges current taxonomic and phylogenetic thoughts, and points towards a reformulation of the genus Citrus."

The researchers analyzed the genomes of 58 members of the Citrus genus and the related genera Fortunella, Eremocitrus, and Microcitrus, as well as two outgroup genera Poncirus and Severinia. Their samples included citrus species that had not previously been sequenced or analyzed, such as the pure mandarin C. reticulata, the citron C. medica, the Nagami kumquat F. margarita, a wild citrus species, and three Australian citrus species.

Based on segmental ancestry and shared haplotypes, the researchers confirmed that grapefruit is a pummelo-sweet orange hybrid, while the lemon is a sour orange-citron hybrid. Additionally, they found that the Rangpur lime and red rough lemon are two different mandarin-citron hybrids and that the calamondin is a kumquat-mandarin hybrid.

Through a combination of diversity analysis, multi-dimensional scaling, and chloroplast genome phylogeny, Wu and his colleagues uncovered 10 progenitor citrus species. A principal components analysis first separated three ancestral Citrus species and associated them with commercially important fruit: citrons, mandarins, and pummelos, and pegged lemons, limes, oranges, and grapefruit as hybrids of those three ancestral species. They also noted extensive relatedness between mandarins and sweet oranges.

Using ancestry-informative markers from citrons, mandarins, and pummelos, the researchers teased out the segmental ancestry of 46 citrus accessions.

Twenty-three of the 28 sequenced mandarins have some pummelo admixture, they found. The amount and pattern of pummelo admixture the mandarins contained separated them into three groups: one with no pummelo admixture, one with a small amount, and one with a high amount of pummelo admixture. This suggested to the researchers that the initial pummelo introgression into mandarins may have been quite small — perhaps even from a single pummelo — and its contribution was diluted through backcrosses to give rise to the second group. The third group then experienced additional introgressions.

The level of pummelo admixture in citrus is linked to both fruit size and acidity. The size of mandarins, oranges, and grapefruit correlates with their proportion of pummelo admixture, the researchers said. Additionally, in mandarins, pummelo introgression appears linked to their palatability, or acid levels.

At the same time, the researchers used nuclear phylogeny — which differed from the chloroplast phylogeny — to trace the origin of citrus. Citrus, they reported, radiated rapidly in Asia during the late Miocene, some six million to eight million years ago, at a time when monsoons in the region weakened and the climate became drier. It spread from Southeast Asia to Australia during the early Pliocene, about four million years ago.

In addition, the Tachibana mandarin, which is found in Taiwan, and Japan, split from mainland Asian mandarins about two million years ago, during the early Pleistocene. Although Tachibana has its own species, the researchers noted that it is closely related to pure mandarins, C. reticulata, though with some differences, and they suggested that Tachibana ought to be categorized as a subspecies of C. reticulata.

They likewise noted that the related genus Poncirus, which has sometimes been classified as part of Citrus, forms a distinct clade.

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