Historical and Scientific Evidence for the Origin and Cultural Importance to Australia’s First-Nations Peoples of the Laboratory Accession of Nicotiana benthamiana, a Model for Plant Virology

Abstract

Nicotiana benthamiana is an indigenous plant species distributed across northern Australia. The laboratory accession (LAB) of N. benthamiana has become widely adopted as a model host for plant viruses, and it is distinct from other accessions morphologically, physiologically, and by having an attenuation-of-function mutation in the RNA-dependent RNA polymerase 1 (NbRdr1) gene, referred to as NbRdr1m. Recent historical evidence suggested LAB was derived from a 1936 collection by John Cleland at The Granites of the Northern Territory, although no scientific evidence was provided. We provide scientific evidence and further historical evidence supporting the origin of LAB as The Granites. Analysis of a herbarium specimen of N. benthamiana collected by Cleland in 1936 revealed that The Granites population contains plants heterozygous for the NbRdr1 locus, having both the functional NbRdr1 and the mutant NbRdr1m alleles. N. benthamiana was an important cultural asset actively utilised as the narcotic Pituri (chewing tobacco) by the Warlpiri Aboriginal people at the site, who prevented women of child-bearing age from consuming it. We propose that Aboriginal people selected some of the unique traits of LAB that have subsequently facilitated its adoption as a model plant, such as lack of seed dormancy, fast maturity, low nornicotine content, and gracility.

Genomic insights into recent species divergence in Nicotiana benthamiana and natural variation in Rdr1 gene controlling viral susceptibility

“…The fact that these populations exhibit variation in the Rdr1 insertion, and some are heterozygous, also raises further questions. Recently, heterozygosity for the insertion was also identified in a herbarium specimen from the original collection in 1936 by Cleland from The Granites Goldmine, where the LAB genotype originated (Wylie & Li, 2022). Presence of the insertion parallels differences in seed size (Table S2), but it does not reduce the time to first flowering and seed release as postulated previously (Bally et al., 2015).…”

“…Wylie and Li (2022) also speculated that the rapid development and other distinctive traits hypothesized by Bally et al. (2015) in the extremophile hypothesis might have been selected by the Aboriginal people: ‘at least some traits distinctive to LAB were consciously selected by the Warlpiri people and their ancestors who used this plant as a narcotic over vast time periods’.…”

“…However, LAB does not stand as an outlier in terms of developmental rapidity, and it is difficult to imagine that the Warlpiri and other native peoples would have selected for the morphological differences in LAB and its relatives. The Wylie and Li (2022) speculation about human selection is largely based on the erroneous conclusions of Bally et al. (2015) and can thus be discounted.…”

“…The remaining species began to diverge only 125 000 years ago, with the most recent split between eWA and WA2 occurring only c. 75 000 years ago, just before the human occupation of Australia began c. 65 000 years ago (Clarkson et al, 2017a). Wylie and Li (2022) also speculated that the rapid development and other distinctive traits hypothesized by Bally et al (2015) in the extremophile hypothesis might have been selected by the Aboriginal people: 'at least some traits distinctive to LAB were consciously selected by the Warlpiri people and their ancestors who used this plant as a narcotic over vast time periods'. However, LAB does not stand as an outlier in terms of developmental rapidity, and it is difficult to imagine that the Warlpiri and other native peoples would have selected for the morphological differences in LAB and its relatives.…”

“…All field-collected material of N. benthamiana was subject to agreement by and in some cases with participation of local people, despite the accusations to the contrary by Wylie and Li (2022). It is covered under the following collecting permits to MWC and MJMC: Western Australia SW017148, CE006044, Northern Territory 58658 and Queensland PTU-18001061.…”