Genome-wide transcriptomic and phylogenetic analyses reveal distinct aluminum-tolerance mechanisms in the aluminum-accumulating species buckwheat (Fagopyrum tataricum)

Abstract

BackgroundSimilar to common buckwheat (Fagopyrum esculentum), tartary buckwheat (Fagopyrum tataricum) shows a high level of aluminum (Al) tolerance and accumulation. However, the molecular mechanisms for Al detoxification and accumulation are still poorly understood. To begin to elucidate the molecular basis of Al tolerance and accumulation, we used the Illumina high-throughput mRNA sequencing (RNA-seq) technology to conduct a genome-wide transcriptome analysis on both tip and basal segments of the roots exposed to Al.ResultsBy using the Trinity method for the de novo assembly and cap3 software to reduce the redundancy and chimeras of the transcripts, we constructed 39,815 transcripts with an average length of 1184 bp, among which 20,605 transcripts were annotated by BLAST searches in the NCBI non-redundant protein database. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that expression of genes involved in the defense of cell wall toxicity and oxidative stress was preferentially induced by Al stress. Our RNA-seq data also revealed that organic acid metabolism was unlikely to be a rate-limiting step for the Al-induced secretion of organic acids in buckwheat. We identified two citrate transporter genes that were highly induced by Al and potentially involved in the release of citrate into the xylem. In addition, three of four conserved Al-tolerance genes were found to be duplicated in tartary buckwheat and display diverse expression patterns.ConclusionsNearly 40,000 high quality transcript contigs were de novo assembled for tartary buckwheat, providing a reference platform for future research work in this plant species. Our differential expression and phylogenetic analysis revealed novel aspects of Al-tolerant mechanisms in buckwheat.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0395-z) contains supplementary material, which is available to authorized users.

Differences in Aluminium Accumulation and Resistance between Genotypes of the Genus Fagopyrum

“…In the study by reference [35] the xylem citrate-concentration did not respond to externally applied or internally transported Al. These results are in agreement with the analysis of the effect of Al on the global transcriptome in F. esculentum [36] and F. tataricum [37] root tips which did not show major effects on genes involved in organic acid metabolism suggesting that citrate was not a rate-limiting step for Al transport into and in the xylem. However, in these studies a major difference in citrate concentration and synthesis between the root cortex and the central cylinder has not been taken into consideration.…”

“…Together with the strong reduction of Fe xylem-sap concentrations by Al ( Figure 7B) this may indicate that both Al and Fe are transported through the same transporter, and Fe transport is competitively inhibited by the more abundant Al (factor ten). The positive correlation between xylem-sap Al and Fe concentrations may then reflect the Al-enhanced transporter abundance in agreement with the higher expression of the genes coding for these transporters [36,37].…”

“…Iron is known to be transported in the xylem coupled to citrate which is loaded into the xylem through MATE/FRD-proteins coded by FRD3 in Arabidopsis [39], OsFRDL1 in rice [40] or HvAACT1 in barley [41]. The above mentioned recent global transcriptome analysis of Al-induced genes in root tips clearly revealed that among the strongly Al up-regulated genes were the homologues of these genes, FtFRDL1 and FtFRDL2 in F. tataricum [37] and FeMATE1 and FeMATE2 in F. esculentum [36]. Their role in citrate and Al loading into the xylem remains to be investigated in the future.…”

“…The genes and proteins (particularly transporters involved in Al exclusion and Al tolerance/accumulation) have still not yet been identified. It is expected that recent transcriptomic studies will pave the way for a better understanding of the molecular basis of Al resistance of buckwheat [36,37,43]. In the model plants Arabidopsis and rice, an interplay between Al exclusion by root exudation of organic acid anions and the rapid uptake and accumulation in the root vacuole has been widely established [17,44].…”

Glutathione S-transferases and UDP-glycosyltransferases Are Involved in Response to Aluminum Stress in Flax

“…Diverse plant species have different strategies for Al resistance; these have been described for various plants, including wheat (Delhaize et al, 1993; Garcia-Oliveira et al, 2013; Moustaka et al, 2016), barley (Furukawa et al, 2007; Ma et al, 2016), sorghum (Magalhaes et al, 2007; Caniato et al, 2014), rice (Ma et al, 2002; Yokosho et al, 2011; Xia et al, 2013; Arenhart et al, 2014), maize (Piñeros et al, 2002; Maron et al, 2013), Arabidopsis (Liu et al, 2009; Mangeon et al, 2016), snap bean (Miyasaka et al, 1991), buckwheat (Zhu et al, 2015), eucalyptus (Tahara et al, 2014), and hydrangea (Negishi et al, 2013). …”