Whole-Transcriptome RNA Sequencing Reveals the Global Molecular Responses and CeRNA Regulatory Network of mRNAs, lncRNAs, miRNAs and circRNAs in Response to Salt Stress in Sugar Beet (Beta vulgaris)

Abstract

Sugar beet is an important sugar-yielding crop with some tolerance to salt, but the mechanistic basis of this tolerance is not known. In the present study, we have used whole-transcriptome RNA-seq and degradome sequencing in response to salt stress to uncover differentially expressed (DE) mRNAs, microRNAs (miRNAs), long non-coding RNAs (lncRNAs) and circular RNAs (circRNAs) in both leaves and roots. A competitive endogenous RNA (ceRNA) network was constructed with the predicted DE pairs, which revealed regulatory roles under salt stress. A functional analysis suggests that ceRNAs are implicated in copper redistribution, plasma membrane permeability, glycometabolism and energy metabolism, NAC transcription factor and the phosphoinositol signaling system. Overall, we conducted for the first time a full transcriptomic analysis of sugar beet under salt stress that involves a potential ceRNA network, thus providing a basis to study the potential functions of lncRNAs/circRNAs.

Salt and Drought Stress Responses in Cultivated Beets (Beta vulgaris L.) and Wild Beet (Beta maritima L.)

“…The miRNAs regulate the expression of their target genes at post-transcriptional level via degradation, and at the post-translational level by inhibition [165,169]. Although the miRNAs are known to be activated in response to stress in plants, similar data from beets have been less abundantly reported [55,170]. Through bioinformatics approach, beet genome was found to encode 13 mature miRNAs, and their targets encode transcription factors, signal transduction components, and factors related to stress response [171].…”

“…In addition to salt tolerance, beets display better tolerance to water deficit compared to other grain crops [ 18 , 23 , 48 , 49 ]. Major abiotic stress factors such as salinity and drought in beets generally cause various morpho-physiological alterations such as growth retardation, wilting of leaves, reduction in stomatal conductance, photosynthetic rate and transpiration, decline in relative water content (RWC), leaf photosynthetic pigments, lower root biomass, membrane damage through lipid peroxidation, accumulation of compatible solutes, lower white sugar yield, and enhancement of specific leaf weight and succulence index [ 18 , 30 , 31 , 50 , 51 , 52 , 53 , 54 , 55 ]. In beets, yield reductions after drought might be due to changes in RWC and water potential in leaves [ 56 ], limited leaf growth and CO 2 assimilation [ 57 ].…”

“…The proline accumulation increased rapidly in different organs of sugar beet, fodder beet, and red beet under salt and drought stress [ 16 , 50 , 71 , 83 ]. For example, in a recent work, it was shown to increase remarkably in leaves but not in roots under high salt stress [ 55 ]. However, fodder beet showed increased proline content in both taproots and leaves under salt stress [ 16 ].…”

“…In contrast to the LKC-2006, higher sucrose accumulation was observed in the roots of salt-tolerant sugar beet genotype (LKC-HB) after 60 days of salt stress [ 61 ]. Moreover, in the sugar beet cultivar (O68), the soluble sugars remarkably enhanced in both leaves and roots at 300 mM NaCl, but the elevation was higher in leaves than in roots [ 55 ]. However, two recent studies have shown reduced sucrose content in sugar beet roots after 1 day of salt stress and in LKC-HB leaves during salinity [ 50 , 61 ].…”

“…In a sugar beet cultivar (HI-0473), the activities of CAT and POX enzymes markedly increased under mild and severe salt concentrations [ 35 ]. Although SOD and POX activities increased in both leaves and roots of sugar beet, an increase in CAT activity was higher in leaves than in roots, and the activity remained high during severe salt stress [ 55 ]. However, the APX activity was decreased in response to severe salinity (150 and 250 mM NaCl), whereas lower salt concentrations (75 and 100 mM NaCl) enhanced the enzyme activity [ 35 ].…”