Beyond the greenhouse: coupling environmental and salt stress response reveals unexpected global transcriptional regulatory networks in Salicornia bigelovii

Abstract

Soil salinity is an increasing threat to global food production systems. As such, there is a need for salt tolerant plant model systems in order to understand salt stress regulation and response. Salicornia bigelovii, a succulent obligatory halophyte, is one of the most salt tolerant plant species in the world. It possesses distinctive characteristics that make it a candidate plant model for studying salt stress regulation and tolerance, showing promise as an economical non-crop species that can be used for saline land remediation and for large-scale biofuel production. However, available S. bigelovii genomic and transcriptomic data are insufficient to reveal its molecular mechanism of salt tolerance. We performed transcriptome analysis of S. bigelovii flowers, roots, seeds and shoots tissues cultivated under desert conditions and irrigated with saline aquaculture effluent. We identified a unique set of tissue specific transcripts present in this non-model crop. A total of 66,943 transcripts (72.63%) were successfully annotated through the GO database with 18,321 transcripts (27.38%) having no matches to known transcripts. Excluding non-plant transcripts, differential expression analysis of 49,914 annotated transcripts revealed differentially expressed transcripts (DETs) between the four tissues and identified shoots and flowers as the most transcriptionally similar tissues relative to roots and seeds. The DETs between above and below ground tissues, with the exclusion of seeds, were primarily involved in osmotic regulation and ion transportation. We identified DETs between shoots and roots implicated in salt tolerance including SbSOS1, SbNHX, SbHKT6 upregulated in shoots relative to roots, while aquaporins (AQPs) were up regulated in roots. We also noted that DETs implicated in osmolyte regulation exhibit a different profile among shoots and roots. Our study provides the first report of a highly upregulated HKT6 from S. bigelovii shoot tissue. Furthermore, we identified two BADH transcripts with divergent sequence and tissue specific expression pattern. Overall, expression of the ion transport transcripts suggests Na⁺ accumulation in S. bigelovii shoots. Our data led to novel insights into transcriptional regulation across the four tissues and identified a core set of salt stress-related transcripts in S. bigelovii.