genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: An example of a naturally transgenic food crop

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-05, Vol.112 (18), p.5844-5849
• Main Authors: Kyndt, Tina, Quispe, Dora, Zhai, Hong, Jarret, Robert, Ghislain, Marc, Liu, Qingchang, Gheysen, Godelieve, Kreuze, Jan F
• Format: Article
• Language: English
• Subjects: Agrobacterium - genetics; Agrobacterium rhizogenes; Agrobacterium tumefaciens; Biological Sciences; Deoxyribonucleic acid; DNA; DNA, Bacterial - genetics; DNA, Plant - genetics; Food Safety; Gene expression; Gene Transfer, Horizontal; Genome, Plant; Genomics; Gram-negative bacteria; Ipomoea batatas; Ipomoea batatas - genetics; Open Reading Frames; Phylogeny; Plant Leaves - metabolism; Plant Roots - metabolism; Plant Shoots - metabolism; Plant Stems - metabolism; Plants, Genetically Modified; Ribonucleic acid; RNA; RNA, Small Interfering - genetics; Sequence Analysis, DNA; Solanum tuberosum; Vegetables
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1419685112

Significance We communicate the rather remarkable observation that among 291 tested accessions of cultivated sweet potato, all contain one or more transfer DNA (T-DNA) sequences. These sequences, which are shown to be expressed in a cultivated sweet potato clone (“Huachano”) that was analyzed in detail, suggest that an Agrobacterium infection occurred in evolutionary times. One of the T-DNAs is apparently present in all cultivated sweet potato clones, but not in the crop’s closely related wild relatives, suggesting the T-DNA provided a trait or traits that were selected for during domestication. This finding draws attention to the importance of plant–microbe interactions, and given that this crop has been eaten for millennia, it may change the paradigm governing the “unnatural” status of transgenic crops. Agrobacterium rhizogenes and Agrobacterium tumefaciens are plant pathogenic bacteria capable of transferring DNA fragments [transfer DNA (T-DNA)] bearing functional genes into the host plant genome. This naturally occurring mechanism has been adapted by plant biotechnologists to develop genetically modified crops that today are grown on more than 10% of the world’s arable land, although their use can result in considerable controversy. While assembling small interfering RNAs, or siRNAs, of sweet potato plants for metagenomic analysis, sequences homologous to T-DNA sequences from Agrobacterium spp. were discovered. Simple and quantitative PCR, Southern blotting, genome walking, and bacterial artificial chromosome library screening and sequencing unambiguously demonstrated that two different T-DNA regions ( Ib T-DNA1 and Ib T-DNA2) are present in the cultivated sweet potato ( Ipomoea batatas [L.] Lam.) genome and that these foreign genes are expressed at detectable levels in different tissues of the sweet potato plant. Ib T-DNA1 was found to contain four open reading frames (ORFs) homologous to the tryptophan-2-monooxygenase ( iaaM ), indole-3-acetamide hydrolase ( iaaH ), C-protein ( C-prot ), and agrocinopine synthase ( Acs ) genes of Agrobacterium spp. Ib T-DNA1 was detected in all 291 cultigens examined, but not in close wild relatives. Ib T-DNA2 contained at least five ORFs with significant homology to the ORF14 , ORF17n , rooting locus ( Rol ) B/RolC , ORF13 , and ORF18/ORF17n genes of A. rhizogenes . Ib T-DNA2 was detected in 45 of 217 genotypes that included both cultivated and wild species. Our finding, that sweet potato is naturally transgenic whi