Alternative Polyadenylation and Salicylic Acid Modulate Root Responses to Low Nitrogen Availability

Abstract

Nitrogen (N) is probably the most important macronutrient and its scarcity limits plant growth, development and fitness. N starvation response has been largely studied by transcriptomic analyses, but little is known about the role of alternative polyadenylation (APA) in such response. In this work, we show that N starvation modifies poly(A) usage in a large number of transcripts, some of them mediated by FIP1, a component of the polyadenylation machinery. Interestingly, the number of mRNAs isoforms with poly(A) tags located in protein-coding regions or 5′-UTRs significantly increases in response to N starvation. The set of genes affected by APA in response to N deficiency is enriched in N-metabolism, oxidation-reduction processes, response to stresses, and hormone responses, among others. A hormone profile analysis shows that the levels of salicylic acid (SA), a phytohormone that reduces nitrate accumulation and root growth, increase significantly upon N starvation. Meta-analyses of APA-affected and fip1-2-deregulated genes indicate a connection between the nitrogen starvation response and salicylic acid (SA) signaling. Genetic analyses show that SA may be important for preventing the overgrowth of the root system in low N environments. This work provides new insights on how plants interconnect different pathways, such as defense-related hormonal signaling and the regulation of genomic information by APA, to fine-tune the response to low N availability.

Interplay between Hormones and Several Abiotic Stress Conditions on Arabidopsis thaliana Primary Root Development

“…Furthermore, in a medium with N-deficient or high N levels, the co-treatment with either trans zeatin (tZ) or cis zeatin (cZ), leads to an important decrement of the PR length compared to control conditions. Interestingly, the tZ treatment causes a major root length reduction than the cZ treatment, in both conditions [210]. Also it has been described that nitrate is able to stimulate PR growth increasing CK biosynthesis and signaling and promoting meristem activity [205].…”

“…Ethylene: The PR growth of plants growing in the co-treatment with ACC in a medium with low or high N levels are shorter than WT plants [210] (Figure 4A).…”

“…Auxin: Under low and high N conditions, the IAA treatment reduces WT PR length compared to plants grown under control conditions. However, this reduction is greater under N deficiency [210]. Curiously, the "transceptor" (transporter/sensor) of NO 3 − , NPF6.3/NRT1.1 (a member of the NRT1/PTR family), can facilitate the uptake of auxin under low NO 3 − concentrations ( Figure 4A) [211].…”

“…GA: Under low (50 µM) and high (2500 µM) N conditions, the GA3 treatment increases the WT PR length compared to control conditions without the hormone treatment ( Figure 4A). However, the PR length is greater under the co-treatment of GA3 and high N [210]. Moreover, the OE of the nitrate transporter of the NRT1/PTR FAMILY (NPF3), a low-affinity nitrate/nitrite transporter that can also transport GA in the root endodermal cells in the EZ, has shorter roots than WT plants.…”

Plant 3’ Regulatory Regions From mRNA-Encoding Genes and Their Uses to Modulate Expression

“…Although we have only just begun to unravel the mechanism, we know that APA has temporal (cell and developmental cycle) and tissue specificity, in addition to being involved in different biological processes, such as embryogenesis, gametogenesis, morphogenesis, control of flowering time in plants and control of oncogenes expression in animals ( Xing and Li, 2011 ; Deridder et al., 2012 ; Tian and Manley, 2016 ; Ji et al., 2018 ). Moreover, APA events are also involved with growth and development ( Hong et al., 2018 ), circadian rhythm ( Yang et al., 2020 ), cell signaling ( Chakrabarti and Hunt, 2015 ; Li et al., 2017 ; Conesa et al., 2020 ), immunity ( Lyons et al., 2013 ; Ye et al., 2019 ) and stress response in plants ( Zheng et al., 2018 ; Conesa et al., 2020 ).…”