The complex genome and adaptive evolution of polyploid Chinese pepper (Zanthoxylum armatum and Zanthoxylum bungeanum)

Abstract

Zanthoxylum armatum and Zanthoxylum bungeanum, known as "Chinese pepper", are distinguished by their extraordinary complex genomes, phenotypic innovation of adaptive evolution and species-special metabolites. Here, we report reference-grade genomes of Z. armatum and Z. bungeanum. Using high coverage sequence data and comprehensive assembly strategies, we derived 66 pseudo-chromosomes comprising 33 homologous phased groups of 2 subgenomes, including from autotetraploid Z. armatum. The genomic rearrangements and two whole-genome duplications creating large (~4.5 Gb) complex genomes with high ratio of repetitive sequences (>82%) and high chromosome number (2n = 4x = 132). Further analysis of the high-quality genomes shed lights on genomic basis of involutional reproduction, allomones biosynthesis and adaptive evolution in Chinese pepper, revealing a high consistent relationship between genomic evolution, environmental factors, and phenotypic innovation. Our study provides genomic resources and new insights for investigating diversification and phenotypic innovation in Chinese pepper, with broader implications for protection of plants under severe environmental changes.

Sichuan Peppercorn and the Birth of Numbing Spices in East Asia

“…For Z. armatum, ancestral populations appear to have been located in frost free Southwest China (Sichuan, Guizhou, and Yunnan) (Feng et al 2020;Hu et al 2023). For Z. armatum, an analysis of divergence events showed that wild accessions of Z. armatum clustered together and possibly diverged from cultivated accessions ~3−5 kya BP (Feng et al 2020).…”

“…individuals in the population samples by geneticists were clonal (Hu et al 2023). It is hypothesized that this trait evolved as a suite of anti-herbivory linked traits during the Miocene (Hu et al 2023).…”

“…individuals in the population samples by geneticists were clonal (Hu et al 2023). It is hypothesized that this trait evolved as a suite of anti-herbivory linked traits during the Miocene (Hu et al 2023). This contrasts with the co-evolution with pollinators in the example of many other angiosperms, where plants develop traits that encourage dispersal by pollinators.…”

“…This contrasts with the co-evolution with pollinators in the example of many other angiosperms, where plants develop traits that encourage dispersal by pollinators. Hu et al (2023) argues that these traits, alongside the biosynthesis of allomones and alkylamides evolved to deter insect herbivory, but also by extension insect pollination. We argue that the long-distance exchange of seeds (that contained genetic material that was identical to the mother plant) contributed to the high levels of genetic diversity seen within Z. bungeanum as cultivars adapted to local conditions as they spread geographically.…”

Karyotype Description and Comparative Chromosomal Mapping of 5S rDNA in 21 species

“…f. species of Orchidaceae (Huan et al 2022); in three Zea L. species of Poaceae (Han et al 2003); in four Citrus L. species of Rutaceae (He et al 2020), Zanthoxylum bungeanum Maxim. and Z. armatum (Hu et al 2023); in four Populus L. species of Salicaceae (Xin et al 2019); in five Taxus L. species of Taxaceae (He et al 2022b).…”