Comparative Genomics and Transcriptomics of the Extreme Halophyte Puccinellia tenuiflora Provides Insights Into Salinity Tolerance Differentiation Between Halophytes and Glycophytes.

Rui Guo,Huiying Lu,Chunwu Yang,Nadeem Bhanbhro,Long Zhao,Kaijian Zhang

doi:10.3389/fpls.2021.649001

Abstract

Halophytes and glycophytes exhibit clear differences in their tolerance to high levels of salinity. The genetic mechanisms underlying this differentiation, however, remain unclear. To unveil these mechanisms, we surveyed the evolution of salinity-tolerant gene families through comparative genomic analyses between the model halophyte Puccinellia tenuiflora and glycophytic Gramineae plants, and compared their transcriptional and physiological responses to salinity stress. Under salinity stress, the K+ concentration in the root was slightly enhanced in P. tenuiflora, but it was greatly reduced in the glycophytic Gramineae plants, which provided a physiological explanation for differences in salinity tolerance between P. tenuiflora and these glycophytes. Interestingly, several K+ uptake gene families from P. tenuiflora experienced family expansion and positive selection during evolutionary history. This gene family expansion and the elevated expression of K+ uptake genes accelerated K+ accumulation and decreased Na+ toxicity in P. tenuiflora roots under salinity stress. Positively selected P. tenuiflora K+ uptake genes may have evolved new functions that contributed to development of P. tenuiflora salinity tolerance. In addition, the expansion of the gene families involved in pentose phosphate pathway, sucrose biosynthesis, and flavonoid biosynthesis assisted the adaptation of P. tenuiflora to survival under high salinity conditions.

Highlights

MATERIALS AND METHODSSoil salinization is a severe environmental problem that limits agricultural production (Flowers and Yeo, 1995; Flowers et al, 2010)
A total of 1, 233 gene families were unique to P. tenuiflora and potentially related to the strong salinity tolerance found in this species (Figure 1B)
The Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment showed that the expanded P. tenuiflora genes were enriched in the plant-pathogen interaction pathway, pentose phosphate pathway (PPP), phenylalanine metabolism, flavone and flavonol biosynthesis, flavonoid biosynthesis, and biosynthesis of amino acids (Figure 2B)

Summary

MATERIALS AND METHODS

Soil salinization is a severe environmental problem that limits agricultural production (Flowers and Yeo, 1995; Flowers et al, 2010). Halophytes and glycophytes exhibit dramatic differences in salinity tolerance, they share most of the characteristics necessary for survival in saline soils These include the control or excretion of Na+ and Cl− in the root, compartmentalization of toxic ions in organs or cells, synthesis of compatible organic solutes in the cytoplasm, and maintenance of sufficient concentrations of key nutrients such as K and N (Flowers and Colmer, 2008; Wang and Xia, 2018). We used MUSCLE software to align the protein sequences of single copy genes in P. tenuiflora, O. sativa, H. vulgare, and A. tauschii (Edgar, 2004) and Gblocks to filter poor positions and transform protein alignments to CDS (Castresana, 2000). We discovered ortholog of each P. tenuiflora gene in the D. glomerata genome using the best BLAST hit based on the CDS sequence (bit score ≥200, E–value ≤−7, and identified ≥60%). The statistical analysis (t-test) of the qRT-PCR and physiological measurements was performed using SPSS 16.0 (SPSS, Chicago, IL, United States)

RESULTS

DISCUSSION

DATA AVAILABILITY STATEMENT