Underground communication: Long non-coding RNA signaling in the plant rhizosphere

Abstract

Long non-coding RNAs (lncRNAs) have emerged as integral gene-expression regulators underlying plant growth, development, and adaptation. To adapt to the heterogeneous and dynamic rhizosphere, plants use interconnected regulatory mechanisms to optimally fine-tune gene-expression-governing interactions with soil biota, as well as nutrient acquisition and heavy metal tolerance. Recently, high-throughput sequencing has enabled the identification of plant lncRNAs responsive to rhizosphere biotic and abiotic cues. Here, we examine lncRNA biogenesis, classification, and mode of action, highlighting the functions of lncRNAs in mediating plant adaptation to diverse rhizosphere factors. We then discuss studies that reveal the significance and target genes of lncRNAs during developmental plasticity and stress responses at the rhizobium interface. A comprehensive understanding of specific lncRNAs, their regulatory targets, and the intricacies of their functional interaction networks will provide crucial insights into how these transcriptomic switches fine-tune responses to shifting rhizosphere signals. Looking ahead, we foresee that single-cell dissection of cell-type-specific lncRNA regulatory dynamics will enhance our understanding of the precise developmental modulation mechanisms that enable plant rhizosphere adaptation. Overcoming future challenges through multi-omics and genetic approaches will more fully reveal the integral roles of lncRNAs in governing plant adaptation to the belowground environment.

Keywords: biotic and abiotic cues; heavy metals; long non-coding RNAs; nutrients; phytoremediation; rhizosphere microbiome.

Figure 1

Overview of lncRNA regulatory functions in mediating plant adaptation responses to biotic and abiotic cues in the rhizosphere environment. As sessile organisms, plants employ sophisticated mechanisms to adapt to their immediate rhizosphere environment for survival. Pathogen detection activates immune signaling cascades, and lncRNAs emerge as integral regulators of plant defenses, including reactive oxygen species, calcium fluxes, hormone pathways, and antimicrobial gene induction. Likewise, lncRNAs enable adaptive plasticity, allowing plants to thrive under stressful rhizosphere conditions such as nutrient deficiencies, contaminant toxicities, and temperature extremes. lncRNAs act as master regulators that perceive external cues and orchestrate specific molecular responses, from restricting uptake to activating detoxification and antioxidant systems. lncRNA, long non-coding RNA; PRR, pattern recognition receptor; NLR, nucleotide-binding domain leucine-rich-repeat-containing receptors; MAPK, mitogen-activated protein kinase; ROS, reactive oxygen species. Created with Biorender.com.

Figure 2

Role of lncRNAs in rhizosphere biotic interactions. (A) In plant–bacteria interactions, lncRNAs modulate the expression of defense mRNAs, playing a role in plant defense by serving as precursors of miRNAs or acting as miRNA sponges. ELENA1 increases Arabidopsis resistance to the bacterial pathogen Pst DC3000 by interacting with the mediator subunit FIB2 and 19a, promoting PR1 gene expression. The lncRNA SUNA1 enhances plant defense against Pst DC3000 by interacting with fibrillarin, thereby improving the pre-rRNA translational and processing efficiency of select defense genes. Furthermore, expression of the SABC1 transporter gene is suppressed upon infection with Pst DC3000. This SABC1 repression triggers downstream transcriptional activation of the NAC3 transcription factor along with genes involved in salicylic acid biosynthesis. Ultimately, silencing of SABC1 leads to elevated salicylic acid levels and enhanced resistance against Pst DC3000. In addition, the lncRNA ALEX1 improves rice resistance against the bacterial pathogen Xanthomonas oryzae pv. oryzae (Xoo). ALEX1 exerts this effect by upregulating jasmonic acid biosynthesis and signaling, as shown by increased endogenous jasmonate levels and increased expression of multiple jasmonic acid-responsive defense genes after ALEX1 induction. (B) lncRNAs mediate plant defense responses against oomycete pathogens through diverse mechanisms, including modulating ROS accumulation, altering expression of pathogenesis-related (PR) genes, and functioning as miRNA decoys. Several positively acting lncRNAs that serve as miRNA target mimics have been shown to enhance plant immunity to oomycetes. By contrast, lncRNA39896 appears to negatively regulate oomycete defense by interfering with miR166 activity and suppressing related antifungal pathways.

Figure 3

Overview of lncRNA-mediated regulation of root-nodule symbiosis. lncRNAs utilize diverse regulatory modes, including miRNA sequestration, protein binding, alteration of RNA-binding protein localization, modulation of translation, and serving as precursors for siRNAs. Characterized examples of lncRNAs involved in root-nodule symbiosis include ENOD40, TAS3, and its alternative isoform ALT TAS3. ENOD40 interacts with MtRBP1, a nuclear speckle RNA-binding protein homolog in M. truncatula, and is proposed to cause MtRBP1 relocalization from the nucleus to the cytoplasm, thus modulating gene expression. TAS3 shows increased association with translational machinery in response to rhizobia. It is predicted to act as a target mimic for miRNA390, subsequently reducing the production of trans-acting small interfering auxin response factors and regulating nodule formation and rhizobial infection.

Figure 4

Deciphering lncRNA regulatory networks and target genes that govern plant cadmium tolerance mechanisms. In Betula platyphylla, the lncRNAs lncRNA2705.1 and lncRNA11415.1 enhance Cd tolerance by regulating the expression of key genes. Specifically, they modulate the heat-shock protein gene HSP18.1, ensuring proteostasis, and the lactate dehydrogenase A (LDHA) gene, promoting redox homeostasis under stress. In addition, the lncRNAs MSTRG.52178.2, MSTRG.21559.1, MSTRG.5307.1, and lncRNA37228 contribute to Cd tolerance by targeting crucial genes, including genes encoding the metal transporter NRAMP3, the reactive oxygen species scavenging enzymes CAT and GPx1, and the D1 subunit of photosystem II involved in photosynthetic electron transport. Another lncRNA, LTCONS00157527, may modulate transporter genes. The barley lncRNAs LTCONS_00177709 and LTCONS_00185175 enhance Cd tolerance by relieving miR319-mediated repression of the master antioxidant regulator HvGAMYB. LTCONS_00015847 confers protection by activating PEX6, stimulating oxidative-damage-control pathways. The poplar lncRNAs MSTRG.5634.1 and MSTRG.22608.1 enhance Cd tolerance and photosynthetic productivity by regulating the MYB transcription factors PtoMYB27 and PtoMYB73, as validated by coordinated expression analysis and Arabidopsis overexpression studies. Various lncRNAs target and potentially regulate genes involved in essential processes. For instance, LOC107279206 targets MYB101, LOC107280054 targets rbcL1, and BGIG39947_32145 targets ANR3, all implicated in the photosynthetic pathway. The rice lncRNA XLOC_086307 and its cis-linked target OS03G0196600, a cysteine/methionine metabolism gene, show coordinated upregulation under Cd exposure, suggesting a role for XLOC_086307 in mediating stress adaptation by directing the production of cysteine-rich peptides. Specific lncRNAs, including LOC107278116 targeting GH9B14 and PGL2, LTCONS00032998 targeting FLA, LTCONS00061453 targeting POD, and LTCONS00114133 targeting SNARE1, are associated with the regulation of cell-wall composition, indicating their involvement in modulation of cellulose, pectin, and overall cell-wall composition. LOC9266110 and LOC9266912 have been linked to hormonal signaling, and TCONS_0003348 targets TC182597, suggesting a role in disease resistance.

Figure 5

lncRNA-mediated communication under Pb²⁺ and Fe stress. (A) The lncRNA PMAT interacts with PtoMYB46 to inhibit the expression of PtoMATE under Pb²⁺ stress in B. platyphylla. Downregulation of PtoMATE decreases the secretion of citric acid and increases the absorption of Pb²⁺. (B) Under low Fe, MSTRG.85814.11 upregulates the expression of its neighboring cis-target gene SAUR32. Increased SAUR32 levels subsequently stimulate transcription of HA10, triggering increased rhizosphere acidification and upregulation of Fe-responsive genes in apple.

Figure 6

lncRNA-related regulatory networks for phosphate homeostasis in plants. (A) The lncRNA IPS1 is induced under phosphate deficiency and acts as a target mimic for miR399 to regulate phosphate homeostasis in Arabidopsis. (B) The cis-natural antisense RNA cis-NATPHO1;2 acts as a translational enhancer for the expression of its sense gene, PHOSPHATE1;2 (PHO1;2), by increasing its association with polysomes to control phosphate homeostasis in rice, but the pathway involved is still unknown.

Figure 7

lncRNAs play pivotal roles in the regulatory networks that govern plant nitrogen homeostasis. Nitrogen deficiency (−N) induces ELENA1 transcription in roots. The resulting ELENA1 transcripts move to shoots, accumulating in young leaves. There, ELENA1 dissociates the MED19a–ORE1 complex, reducing the recruitment of RNA Pol II to promoters. This attenuation of ORE1 target expression enables ELENA1 to regulate −N-induced leaf senescence. In addition, miR858 expression in leaves is substantially increased under low-nitrogen conditions compared with control conditions. The increased level of miR858 prevents eTM858-1 and eTM858-2 from reducing miR858’s cleavage of MsMYB62-like. This reduction in MsMYB62-like expression alleviates inhibition of the MsF3′H promoter, promoting anthocyanin biosynthesis. The lncRNA T5120 plays a role in NLP7 nitrate regulation in plant roots; NLP7 binds to an NRE-like motif in the T5120 promoter when nitrate is present, controlling its expression. In barley race B968 under nitrogen deficiency, lnc00090 and lnc000248 act as miR399 target mimics, implying that miR399 assists with nitrogen deficiency responses. Similarly, expression of the lncRNA IPS1 is altered under both nitrogen and phosphate deprivation. Expression analysis has revealed upregulation of the RHC-class lncRNA Chr04G0017 in rice roots under nitrogen and phosphorus deficiency. Finally, the cis-NAT lncRNA–mRNA pairs cis_NATAMT1.1/AMT1.1 and cis_NATAMT1.2/AMT1.2 exhibit distinct regulatory behaviors in rice under low-nitrogen conditions. Whereas cis_NATAMT1.2 and AMT1.2 display root-specific co-expression, cis_NATAMT1.1 and AMT1.1 show divergent tissue-specific expression.