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Genome-Wide Analysis of Nucleotide-Binding Site (NBS) Disease Resistance (R) Genes in Sacred Lotus (Nelumbo nucifera Gaertn.) Reveals Their Transition Role During Early Evolution of Land Plants

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Abstract

Nucleotide-binding site (NBS) containing genes comprise the largest class in identified plant resistance genes. A total of 137 NBS class resistance genes were identified from the newly sequenced sacred lotus genome (Nelumbo nucifera Gaertn.) through a reiterative computational sequence analysis. Three distinct groups of NBS-encoding genes were classified: 5 with Toll/interleukin-1 receptor homology (TIR) domain at N-terminal (TIR-NBS [-LRR (leucine-rich repeat)]), 37 with CC (coiled coil) domain (CC-NBS [-LRR]), and 95 with neither TIR nor CC at N-terminal (NBS [-LRR]). Sequence analysis revealed high divergence of NBS-LRR genes in sacred lotus. The result of cluster and syntenic analysis of NBS genes suggested a duplication and recombination event, which is consistent with the correspondent result of whole genome analysis. In addition, we also identified 52 NBS genes which have a putative NACHT domain embedded in the NBS domains. This characteristic has only been reported in animals, fungi and bacteria, suggesting that NACHT and NBS domains shared a similar ancient origin; and sacred lotus NBS (NACHT) genes may represent a transition role during the early evolution of disease resistance in land plants.

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Abbreviations

NBS:

Nucleotide-binding site

NB-ARC:

NB, ARC1, and ARC2

NACHT:

NAIP, CIITA, HET-E, and TP1

TIR:

Toll/interleukin-1 receptor (TIR) homology domain

CC:

Coiled coil domain

LRR:

Leucine-rich repeat

R:

Resistance

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Acknowledgments

We thank Dr. Ming-Li Wang at the Hawai‘i Agriculture Research Center (HARC) for providing assistance with bioinformatics and Dr. Heather McCafferty at HARC for critical reviewing of the manuscript. This work was supported partially by a cooperative agreement (No. CA 58-5320-3-460) between the U.S. Department of Agriculture-Agricultural Research Service and HARC.

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Authors and Affiliations

  1. Hawaii Agriculture Research Center, P. O. Box 100, Kunia, HI, 96759, USA

    Rui Zong Jia & Yun J. Zhu

  2. Department of Plant Biology, University of Illinois, Urbana, IL, 61801, USA

    Ray Ming

  3. Institute of Tropical Bioscience and Biotechnology, China Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, People’s Republic of China

    Yun J. Zhu

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  1. Rui Zong Jia
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  2. Ray Ming
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Correspondence to Yun J. Zhu.

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Communicated by Paul Arruda

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Supplementary Table 1

Putative NACHT domains embedded in NB-ARC domains among the predicted R genes. (DOC 164 kb)

Supplementary Table 2

List of syntenic pairs among the NBS encoding genes. (DOC 36 kb)

Supplementary Figure 1

Divergence analysis of NBS (NB-ARC and NACHT domains). A Neighbor-joining tree was constructed from distance matrices. The main branch grouped in shadow represents the NBS genes from different organisms showing similarity. The number next to the branch indicates the percentage of 1,000 bootstrap replicates, but some were not reported. Except for those proteins predicted from sacred lotus headed by “NNU”, the sacred lotus genes ended with “A” or “B” indicating NACHT, or NB-ARC. All the other NBS encoding proteins were randomly imported from Pfam database, and a unique accession number (UniProtKB/Swiss-Prot, www.uniprot.org) follows the abbreviation of the species name in brackets. Abbreviations of plant names were the same as these presented in Table 1, except, Am indicates Ailuropoda melanoleuca (Giant panda), Hs indicates Homo sapiens (Human), Mm for Mus musculus (Mouse), Ss for Sus scrofa (Pig), and Dr for Danio rerio (Zebrafish). (PPT 304 kb)

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Jia, R.Z., Ming, R. & Zhu, Y.J. Genome-Wide Analysis of Nucleotide-Binding Site (NBS) Disease Resistance (R) Genes in Sacred Lotus (Nelumbo nucifera Gaertn.) Reveals Their Transition Role During Early Evolution of Land Plants. Tropical Plant Biol. 6, 98–116 (2013). https://doi.org/10.1007/s12042-013-9122-4

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