Pi-starvation induced transcriptional changes in barley revealed by a comprehensive RNA-Seq and degradome analyses

Abstract

Background Small RNAs (sRNAs) are 20–30 nt regulatory elements which are responsible for plant development regulation and participate in many plant stress responses. Insufficient inorganic phosphate (Pi) concentration triggers plant responses to balance the internal Pi level. Results In this study, we describe Pi-starvation-responsive small RNAs and transcriptome changes in barley (Hordeum vulgare L.) using Next-Generation Sequencing (NGS) RNA-Seq data derived from three different types of NGS libraries: (i) small RNAs, (ii) degraded RNAs, and (iii) functional mRNAs. We find that differentially and significantly expressed miRNAs (DEMs, Bonferroni adjusted p-value < 0.05) are represented by 15 molecules in shoot and 13 in root; mainly various miR399 and miR827 isomiRs. The remaining small RNAs (i.e., those without perfect match to reference sequences deposited in miRBase) are considered as differentially expressed other sRNAs (DESs, p-value Bonferroni correction < 0.05). In roots, a more abundant and diverse set of other sRNAs (DESs, 1796 unique sequences, 0.13% from the average of the unique small RNA expressed under low-Pi) contributes more to the compensation of low-Pi stress than that in shoots (DESs, 199 unique sequences, 0.01%). More than 80% of differentially expressed other sRNAs are up-regulated in both organs. Additionally, in barley shoots, up-regulation of small RNAs is accompanied by strong induction of two nucleases (S1/P1 endonuclease and 3′-5′ exonuclease). This suggests that most small RNAs may be generated upon nucleolytic cleavage to increase the internal Pi pool. Transcriptomic profiling of Pi-starved barley shoots identifies 98 differentially expressed genes (DEGs). A majority of the DEGs possess characteristic Pi-responsive cis-regulatory elements (P1BS and/or PHO element), located mostly in the proximal promoter regions. GO analysis shows that the discovered DEGs primarily alter plant defense, plant stress response, nutrient mobilization, or pathways involved in the gathering and recycling of phosphorus from organic pools. Conclusions Our results provide comprehensive data to demonstrate complex responses at the RNA level in barley to maintain Pi homeostasis and indicate that barley adapts to Pi-starvation through elicitation of RNA degradation. Novel P-responsive genes were selected as putative candidates to overcome low-Pi stress in barley plants.

Comparative Omics Analysis of Brassica napus Roots Subjected to Six Individual Macronutrient Deprivations Reveals Deficiency-Specific Genes and Metabolomic Profiles

“…In many plant species, several studies have shown that the majority of DEGs identified in K-starved plants are linked to phytohormones (especially auxin and jasmonate), cation transporters (especially iron, zinc, and Ca transporters), Ca signaling, and protein phosphorylation [ 33 , 34 , 35 , 36 , 37 ]. Concerning transcriptomic analysis of P-starved plants, a study performed on wheat identified several DEGs associated with plant defense, plant stress responses, nutrient mobilization, or pathways involved in the gathering and recycling of phosphorus [ 38 ]. In another study authors reported that among the 1644 DEGs in roots of P-deprived plants, most of them belonged to pathways involving phosphorylated metabolites such as nucleic acids and phospholipids [ 39 ].…”

A phosphatase gene is linked to nectar dihydroxyacetone accumulation in mānuka (Leptospermum scoparium)

“…AtSgpp expression is responsive to abiotic stresses, with inorganic phosphate (Pi) starvation causing one of the largest inductions of expression (Caparrós‐Martín et al ., 2013). In wider studies of HAD genes, they have been found to be upregulated in response to Pi stress (Sega et al ., 2021) and contain a high frequency of Pi responsive cis elements in their promoters (Du et al ., 2021). The physiological function of AtSGPP is thought to be housekeeping detoxification, modulation of sugar‐phosphate balance and Pi homeostasis (Caparrós‐Martín et al ., 2013; He et al ., 2019).…”

The RNAome landscape of tomato during arbuscular mycorrhizal symbiosis reveals an evolving RNA layer symbiotic regulatory network

“…Phosphate (Pi) is the most important mineral element delivered by AMF to the host plant. Previous studies have shown that miR399 responds to stress induced by low phosphorus in monocot and dicot plants ( Fujii et al., 2005 ; Bari et al., 2006 ; Chiou et al., 2006 ; Du et al., 2018 ; Sega et al., 2021 ). The results suggest that miR399 may be involved in AMS regulation by balancing Pi uptake pathways.…”