Systems-wide analysis of manganese deficiency-induced changes in gene activity of Arabidopsis roots

Abstract

Manganese (Mn) is pivotal for plant growth and development, but little information is available regarding the strategies that evolved to improve Mn acquisition and cellular homeostasis of Mn. Using an integrated RNA-based transcriptomic and high-throughput shotgun proteomics approach, we generated a comprehensive inventory of transcripts and proteins that showed altered abundance in response to Mn deficiency in roots of the model plant Arabidopsis. A suite of 22,385 transcripts was consistently detected in three RNA-seq runs; LC-MS/MS-based iTRAQ proteomics allowed the unambiguous determination of 11,606 proteins. While high concordance between mRNA and protein expression (R = 0.87) was observed for transcript/protein pairs in which both gene products accumulated differentially upon Mn deficiency, only approximately 10% of the total alterations in the abundance of proteins could be attributed to transcription, indicating a large impact of protein-level regulation. Differentially expressed genes spanned a wide range of biological functions, including the maturation, translation, and transport of mRNAs, as well as primary and secondary metabolic processes. Metabolic analysis by UPLC-qTOF-MS revealed that the steady-state levels of several major glucosinolates were significantly altered upon Mn deficiency in both roots and leaves, possibly as a compensation for increased pathogen susceptibility under conditions of Mn deficiency.

Alternative Splicing Plays a Critical Role in Maintaining Mineral Nutrient Homeostasis in Rice (Oryza sativa)

“…A recent study (Nishida et al, 2017) identified several SR genes that were transcriptionally regulated by N and K deficiency stress, but AS of SR genes was not investigated under nutrient stress. By contrast, a genome-wide analysis in Arabidopsis found that the abundance of several SRs was altered at the protein level but not at the transcriptional level under Mn deficiency (Rodríguez-Celma et al, 2016). Our analysis showed that most rice SR genes (15 out of 22) were differentially alternatively spliced, but not differentially expressed under mineral deficiency.…”

“…As only two studies on Arabidopsis (Yang et al, 2008;Rodríguez-Celma et al, 2016) are available and no -Mn transcriptomic analysis has been reported in rice, we compared our -Mn DEGs with Arabidopsis -Mn genes. We found that, similar to Arabidopsis, the glucosinolate metabolism pathway was enriched in rice DEGs under -Mn, as were several Fe-marker genes such as TOM1 and ENA1 that were antagonistically regulated by deficiencies of Fe and Mn, suggesting that crosstalk occurs between the acquisition responses of the two nutrients, as proposed previously for Arabidopsis (Rodríguez-Celma et al, 2016). In our GO enrichment of DEG analyses, we found a significant enrichment in genes associated with the response to biotic stimulus and cellular detoxification among DEGs identified for plants grown under -Mn conditions.…”

Manganese in Plants: From Acquisition to Subcellular Allocation

“…This review pointed out some transcriptional changes of Mn transporter-encoding genes under Mn-toxic and Mn-deficient conditions, but the signaling networks that underlie these changes are still missing. Furthermore, a recent systems-wide analysis indicated that Mn deficiency responses are primarily regulated at the posttranscriptional level (Rodríguez-Celma et al, 2016). Moreover, our understanding of how Mn transport proteins are regulated is very rudimentary.…”

Effects of Fe and Mn deficiencies on the protein profiles of tomato ( Solanum lycopersicum ) xylem sap as revealed by shotgun analyses

“…Comparative proteomics can provide useful information not only about processes occurring in xylem sap during the adaptation to nutrient stresses, but also can help to target proteins putatively involved in systemic regulation for future studies [47,48]. A significant number of proteomic studies have focused into the effect on different sub-proteomes of nutrient stresses such as Fe (see [49,50] for reviews) and Mn [51,52], but the number of proteomic studies devoted to the effect of nutrient deficiencies and/or toxicities in the xylem sap has been limited, to the best of our knowledge, to studies on the effects of salt stress, K deficiency and N starvation or overload [53][54][55].…”

“…Among the GHs decreasing in abundance, two belong to GH families 10 and 17 (xylanases and endoglucanases) involved in cellulose and xylan degradation whereas three more belong to GH 19,20 and conditions. An antagonistic regulation of Mn and Fe acquisition has been recently proposed to occur in a genomics and proteomics study on whole Arabidopsis roots [52]. The Arabidopsis orthologue of K4D0Y5 (AtSKM1, At2g25790) participates in the CLE45 signaling pathway [84,…”