The genome sequence of the North-European cucumber (Cucumis sativus L.) unravels evolutionary adaptation mechanisms in plants

Abstract

Cucumber (Cucumis sativus L.), a widely cultivated crop, has originated from Eastern Himalayas and secondary domestication regions includes highly divergent climate conditions e.g. temperate and subtropical. We wanted to uncover adaptive genome differences between the cucumber cultivars and what sort of evolutionary molecular mechanisms regulate genetic adaptation of plants to different ecosystems and organism biodiversity. Here we present the draft genome sequence of the Cucumis sativus genome of the North-European Borszczagowski cultivar (line B10) and comparative genomics studies with the known genomes of: C. sativus (Chinese cultivar--Chinese Long (line 9930)), Arabidopsis thaliana, Populus trichocarpa and Oryza sativa. Cucumber genomes show extensive chromosomal rearrangements, distinct differences in quantity of the particular genes (e.g. involved in photosynthesis, respiration, sugar metabolism, chlorophyll degradation, regulation of gene expression, photooxidative stress tolerance, higher non-optimal temperatures tolerance and ammonium ion assimilation) as well as in distributions of abscisic acid-, dehydration- and ethylene-responsive cis-regulatory elements (CREs) in promoters of orthologous group of genes, which lead to the specific adaptation features. Abscisic acid treatment of non-acclimated Arabidopsis and C. sativus seedlings induced moderate freezing tolerance in Arabidopsis but not in C. sativus. This experiment together with analysis of abscisic acid-specific CRE distributions give a clue why C. sativus is much more susceptible to moderate freezing stresses than A. thaliana. Comparative analysis of all the five genomes showed that, each species and/or cultivars has a specific profile of CRE content in promoters of orthologous genes. Our results constitute the substantial and original resource for the basic and applied research on environmental adaptations of plants, which could facilitate creation of new crops with improved growth and yield in divergent conditions.

Figure 1. Schematic representation of chromosomal rearrangements between cucumber varieties.

Figure shows chromosomal localization of inversions and translocations between genomic sequences anchored on chromosomes I–VII and a comparison between the B10 and 9930 lines (chromosome numbering is according to the Borszczagowski karyotype (brackets contain Chinese Long karyotype numbering)). a - Chromosome 1 (4), b - Chromosome 2, c – Chromosome 3, d – Chromosome 4 (6), e – Chromosome 5 (1), f – Chromosome 6 (5), g – Chromosome 7. The top panel bar represents B10 chromosome with scaffolds, the bottom bar represents 9930 chromosome with. The lines show chromosomal rearrangements between sequences of two genomes.

Figure 2. Comparison of CRE content in orthologous genes and freezing tolerance tests of non-acclimated A. thaliana and C. sativus seedlings after abscisic acid (ABA) treatment.

(A) Venn diagrams presenting the number of common and different orthologous genes' groups (5,971) with respect to the occurrences of ABREs, DREs, EREs and their combinations in promoters in A. thaliana, P. trichocarpa, O. sativa and lines B10 and 9930 of northern European and Chinese C. sativus varieties. Total number of orthologous groups with specific CRE or combination of CREs is given in brackets. (B) Freezing tolerance tests of non-acclimated A. thaliana and C. sativus plants after ABA treatment. Leaves were frozen in different temperatures and cellular damage was assessed by measuring electrolyte leakage. Statistically significant difference was assessed by Student's t-test – n = 5, * p-Value<0.05; ** p-Value<0.005. Error bars indicate standard deviations. C – control non-treated plants; ABA – abscisic acid treated plants.