Reexamining a Host-Associated Genomic Diversity of Bean Golden Mosaic Virus (BGMV) Isolates from Phaseolus Species and Other Fabaceae Hosts

Abstract

Beans (Phaseolus vulgaris and P. lunatus) are the major hosts of bean golden mosaic begomovirus (BGMV). Robust taxonomic criteria were established for Begomovirus species demarcation. However, DNA-A identities among BGMV isolates display a continuous variation (89-100%), which conflicts with the current concept of a single viral species. The diversity of 146 Brazilian isolates designated in the GenBank as BGMV was assessed by comparing their complete DNA-A sequences. The isolates were clustered into four groups, being discriminated mainly by their original Fabaceae hosts. Additional Sequence Demarcation Tool analyses indicated that BGMV-related viruses comprise two clear-cut groups: isolates reported infecting mainly P. vulgaris (identities of 96-97% to the reference NC_004042 isolate) and a group associated with P. lunatus (identities of 89-91%). Moreover, we recognized a distinct set of genomic features in the iterons and Rep-associated protein motifs across these two diversity groups. The host prevalence and genomic differences suggest that most P. lunatus isolates are currently misclassified as BGMV strains, being more likely samples of a closely related (but distinct) Begomovirus species. Hence, the implications of this BGMV diversity should be taken into consideration by classical and biotech breeding programs aiming for large-spectrum viral resistance in Phaseolus species.

Keywords: Begomovirus; common bean; lima bean; sequence demarcation tool.

Figure 1

Phylogenetic tree of a set of complete genomes of DNA–A components showing the phylogenetic identities/distances of a subset of 88 out of 146 bean golden mosaic virus (BGMV) isolates available at the GenBank. Midpoint–rooted ML with 1000 bootstrap replications. Group #1 was composed by BGMV isolates reported infecting Phaseolus vulgaris, soybean (Glycine max) and Macroptilium erythroloma (with branches in purple), GenBank accessions (Supplementary Table S1); Group #2 was composed of BGMV isolates obtained from M. lathyroides (with branches in blue); Group #3 was composed of BGMV isolates obtained from P. lunatus (with branches in green); Group #4 was composed by two highly divergent BGMV isolates reported infecting the weed M. lathyroides (with branches in pink). The complete set of information for all 146 isolates is provided in Supplementary Table S1.

Figure 2

Pairwise identity analysis with the Sequence Demarcation Tool (SDT) was carried out using the sequence information of the DNA–A component of a subset of 88 out of 146 isolates obtained from Phaseolus vulgaris, Macroptilium lathyroides, M. erythroloma, and Glycine max indicating their identities in relation to the sequence of the reference (NC_004042) bean golden mosaic virus (BGMV) isolate (highlighted in red font color). BGMV isolates from Phaseolus vulgaris are identified by a numerical order and they correspond to the following GenBank accessions: Phaseolus vulgaris isolates (Pv): 01 (KJ939839), 02 (KJ939838), 03 (KJ939810), 04 (KJ939848), 05 (KJ939829), 06 (KJ939836), 07 (KJ939786), 08 (KJ939815), 09 (KJ939845), 10 (KJ939837), 11 (KJ939822), 12 (KJ939824), 13 (KJ939832), 14 (KJ939823), 15 (KJ939811), 16 (KJ939798), 17 (KJ939841), 18 (KJ939809), 19 (KJ939816), 20 (KJ939801), 21 (KJ939805), 22 (KJ939795), 23 (KJ939813), 24 (KJ939849), 25 (KJ939852), 26 (KJ939818), 27 (KJ939781), 28 (KJ939840), 29 (KJ939783), 30 (KJ939782), 31 (KJ939803), 32 (KJ939842), 33 (KJ939853), 34 (KJ939793), 35 (KJ939812), 36 (MG334552), 37 (KJ939843), 38 (KJ939851), 39 (KJ939792), 40 (KJ939802), 41 (KJ939850), 42 (KJ939799), 43 (KJ939806), 44 (KJ939844), 45 (KJ939826), 46 (KJ939847), 47 (KJ939835), 48 (KJ939830), 49 (KJ939821), 50 (KJ939831), 51 (KJ939819), 52 (KJ939825), 53 (KJ939827), 54 (KJ939788), 55 (KJ939787), 56 (KJ939785), 57 (KJ939820), 58 (KJ939833), 59 (KJ939828), 60 (KJ939780), 61 (KJ939784), 62 (KJ939790), 63 (KJ939779), 64 (KJ939817), 65 (KJ939800), 66 (KJ939789), 67 (KJ939794), 68 (KJ939807), 69 (KJ939808), 70 (KJ939791), 71 (KJ939796), 72 (KJ939797), 73 (KJ939814), 74 (KJ939804), 75 (KJ939834) and 76 (KJ939846); Macroptilium erythroloma isolate (Me) (MN822294); Glycine max isolate (Gm); (FJ665283); Macroptilium lathyroides isolates (Ml): 01 (KJ939725), 02 (KJ939714), 03 (KJ939707), 04 (KJ939756), 05 (KJ939708), 06 (KJ939732), 07 (KJ939764), 08 (KJ939733), 09 (KJ939709), 10 (KJ939717), 11 (KJ939715), 12 (KJ939734)].