Comparative genomics of six Juglans species reveals disease‐associated gene family contractions

Abstract

† These authors are joint first authors. SUMMARYJuglans (walnuts), the most speciose genus in the walnut family (Juglandaceae), represents most of the family's commercially valuable fruit and wood-producing trees. It includes several species used as rootstock for their resistance to various abiotic and biotic stressors. We present the full structural and functional genome annotations of six Juglans species and one outgroup within Juglandaceae (Juglans regia, J. cathayensis, J. hindsii, J. microcarpa, J. nigra, J. sigillata and Pterocarya stenoptera) produced using BRAKER2 semi-unsupervised gene prediction pipeline and additional tools. For each annotation, gene predictors were trained using 19 tissue-specific J. regia transcriptomes aligned to the genomes. Additional functional evidence and filters were applied to multi-exonic and mono-exonic putative genes to yield between 27 000 and 44 000 high-confidence gene models per species. Comparison of gene models to the BUSCO embryophyta dataset suggested that, on average, genome annotation completeness was 85.6%. We utilized these high-quality annotations to assess gene family evolution within Juglans, and among Juglans and selected Eurosid species. We found notable contractions in several gene families in J. hindsii, including disease resistance-related wall-associated kinase (WAK), Catharanthus roseus receptor-like kinase (CrRLK1L) and others involved in abiotic stress response. Finally, we confirmed an ancient whole-genome duplication that took place in a common ancestor of Juglandaceae using site substitution comparative analysis.

Improved de novo chromosome‐level genome assembly of the vulnerable walnut tree Juglans mandshurica reveals gene family evolution and possible genome basis of resistance to lesion nematode

“…The genome of J. regia contained expanded in 2025 gene families, contracted in 243, and 57 were rapidly evolving gene families (+50/−7; Figure 4c; Table S18). In a comparison of the two walnut genomes, we found that gene families associated with pathogen resistance, including wall-associated receptor kinase (WAK;Trouern-Trend et al, 2020), late embryogenesis abundant protein (LEA; Gao et al, 2020), pathogenesis-related protein (PR; Ozyigit et al, 2017;Soh et al, 2012;Zhao et al, 2015), and PPR repeat (PPR; et al, 2016) were significantly contracted (rapidly evolving; family-wide p-value ≤ .01) in J. mandshurica (Figure 4d; Table S18). The nine plant species genomes we studied in detail were highly divergent in terms of the amount of expansion or contraction in these four gene families; even the closely related species J. regia and J. mandshurica were markedly different in terms of levels of expansion.…”

“…The population genetics, morphology, and diversity of J. mandshurica have been described (Aradhya et al, 2007;Dang et al, 2015;Hu et al, 2017;Liu et al, 2020;Manning, 1978;Zhang et al, 2019), but in general, interest in J. mandshurica based on its potential as a tertiary germplasm pool for improvement of J. regia (Chen et al, 2015;Hu et al, 2016;Ji et al, 2020;Trouern-Trend et al, 2020;Zhou et al, 2017). Wild populations of J. mandshurica and cultivated orchards of Persian walnut (J. regia) grow sympatrically (Dang et al, 2019) but hybridization between these two walnut species is reportedly rare (Shu et al, 2016).…”

“…J. mandshurica is less valuable as a commodity than its close relative J. regia (Dang et al, 2016;Feng et al, 2018;Han et al, 2016). However, J. mandshurica expresses horticultural traits such as cluster bearing habit (6-13 fruits per terminal) that make it attractive to J. regia breeders, and disease tolerance/resistance to lesion nematodes (Pratylenchus vulnus) that recommend it as a rootstock for J. regia (Chen et al, 2015;Hu et al, 2016;Ji et al, 2020;Trouern-Trend et al, 2020;Zhou et al, 2017). J. mandshurica is also a potential medicinal crop because of its flavonoids (Bi et al, 2016;Sun et al, 2012;Yu et al, 2011).…”

Antioxidant and antibacterial activities of Pterocarya stenoptera bark extract and its mechanism on Staphylococcus aureus through cell membrane damage

“…Pterocarya stenoptera C. DC. is a native deciduous tree of the maple genus in the Juglans family (Trouern-Trend et al 2020). It is primarily found in the forests along streams, river beaches, and wet mountain slopes below 1500 meters above sea level in China and the Korean Peninsula.…”

De novo chromosome-level genome assembly of Chinese walnut (Juglans cathayensis Dode)

“…It is a diploid plant with 16 chromosomes (2n = 2x = 32) that belongs to the group of species called Asian butternuts (section Cardiocaryon ) that also includes Japanese walnut (J. ailantifolia ) and Manchurian walnut (J. mandshurica ) ( Figure 1; Zhao et al, 2018;Bai et al, 2016;Zhao et al, 2014). Chinese walnut is less valuable as a commodity than its close relative, Juglans regia (Persian or common walnut; Han et al, 2016;Dang et al, 2016;Feng et al, 2018), but Chinese walnut has been evaluated in breeding programs for its resistance to lesion nematodes (Trouern-Trend et al, 2020). In addition, Chinese walnut has potential as a medicinal crop (Yu et al, 2011;Li et al, 2013;Li et al, 2008;Sun et al, 2012;Bi et al, 2016).…”