Abstract

The Great Himalayan Mountains and their foothills are believed to be the place of origin and development of many plant species. The genetic basis of adaptation to high plateaus is a fascinating topic that is poorly understood at the population level. We comprehensively collected and sequenced 377 accessions of Prunus germplasm along altitude gradients ranging from 2,067 to 4,492m in the Himalayas. We de novo assembled three high-quality genomes of Tibetan Prunus species. A comparative analysis of Prunus genomes indicated a remarkable expansion of the SINE retrotransposons occurred in the genomes of Tibetan species. We observed genetic differentiation between Tibetan peaches from high and low altitudes and that genes associated with light stress signaling, especially UV stress signaling, were enriched in the differentiated regions. By profiling the metabolomes of Tibetan peach fruit, we determined 379 metabolites had significant genetic correlations with altitudes and that in particular phenylpropanoids were positively correlated with altitudes. We identified 62 Tibetan peach-specific SINEs that colocalized with metabolites differentially accumualted in Tibetan relative to cultivated peach. We demonstrated that two SINEs were inserted in a locus controlling the accumulation of 3-O-feruloyl quinic acid. SINE1 was specific to Tibetan peach. SINE2 was predominant in high altitudes and associated with the accumulation of 3-O-feruloyl quinic acid. These genomic and metabolic data for Prunus populations native to the Himalayan region indicate that the expansion of SINE retrotransposons helped Tibetan Prunus species adapt to the harsh environment of the Himalayan plateau by promoting the accumulation of beneficial metabolites.

Highlights

  • The Great Himalayan Mountains and their foothills are believed to be the centers of origin and genetic diversity for many cultivated plant species.[1,2] The genetics of adaptation to the extreme Himalayan climate have been reported for several animal species.[3,4,5,6,7,8,9,10,11] for plants, especially perennials, the genetic basis of adaptation to such conditions is largely unknown

  • Collection of Prunus germplasm and survey of their habitual environments on the Tibetan Plateau From 2017 to 2019, we conducted a survey of Tibetan Prunus germplasm around the Himalayan region, including Lhasa

  • A total of 377 Prunus accessions that included 346 peach accessions (299 P. mira, 44 P. persica, 2 P. ferganensis, and 1 P. davidiana), 22 P. avium accessions, 7 P. armeniaca ‘‘Tibet’’ accessions, 1 P. mume ‘‘Tibet’’ accession, and 1 P. salicina ‘‘Tibet’’ accession were collected in this study (Figure S2; Data S1A, S2, and S3)

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Summary

Introduction

The Great Himalayan Mountains and their foothills are believed to be the centers of origin and genetic diversity for many cultivated plant species.[1,2] The genetics of adaptation to the extreme Himalayan climate have been reported for several animal species.[3,4,5,6,7,8,9,10,11] for plants, especially perennials, the genetic basis of adaptation to such conditions is largely unknown. The low-altitude Himalayas are an optimal agro-climatic zone for the production of tree species.[12,13] Particular primitive Prunus species were uniquely distributed in this region.[14,15]. (Rosaceae) consists of over 200 species that include economically important fruit crops,[16] such as peach (Prunus persica), almond (P. dulcis), plum (P. salicina), apricot (P. armeniaca), Mei (P. mume), and sweet cherry (P. avium). Prunus species are widely distributed in the temperate zone of the Northern Hemisphere and in the subtropical and tropical forests of Asia, Africa, South America, and Australia.[16] Wild peach, plum, apricot, and Mei (P. mira, P. salicina ‘‘Tibet,’’ P. armeniaca ’’Tibet,’’ and P. mume ‘‘Tibet’’) were found on the Tibetan Plateau during long-term field investigations. Tibetan peach (P. mira) is probably an ancient progenitor of cultivated peach[18,19] and is endemic to the middle- to high-altitude regions of the Himalayas, at approximately 2,000

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