Long Non-coding RNAs Regulate the Expression of Leucine-rich Repeat Receptor-like Kinases in Plants

Core Concepts

Cis-acting long non-coding RNAs (cis-NATs) are central regulators of leucine-rich repeat receptor-like kinase (LRR-RLK) expression and function in plants.

Abstract

This study investigates the widespread association between long non-coding RNAs (lncRNAs) and the large family of leucine-rich repeat receptor-like kinases (LRR-RLKs) in plants. The key findings are:

The majority of LRR-RLK genes in Arabidopsis, tomato, and rice are associated with cis-acting long non-coding RNAs (cis-NATs) transcribed from the antisense strand. This association is highly conserved across plant evolution.

Overexpression of cis-NATs associated with well-studied LRR-RLKs (BRI1, CLV1, SOBIR1) leads to functional phenotypes that mimic the loss-of-function mutants of the cognate LRR-RLKs. This demonstrates that cis-NATs can regulate LRR-RLK expression and activity.

The promoters of cis-NATs show distinct spatial and temporal expression patterns, suggesting they can fine-tune LRR-RLK expression in a cell-autonomous manner. Targeting cis-NAT expression to specific tissues confirms their cell-autonomous regulatory function.

The widespread and conserved association between LRR-RLKs and cis-NATs across plant species indicates that this regulatory mechanism serves an important and ancient purpose in plants, likely to enable precise control of this critical receptor family.

Overall, this study uncovers cis-NATs as a key regulatory layer that fine-tunes the expression and function of LRR-RLKs, a large family of receptors that are central to plant growth, development, and immunity.

Stats

The majority of LRR-RLK genes in Arabidopsis (212/225, ~94%), tomato (54/232, ~23%), and rice (63/316, ~20%) are associated with cis-acting long non-coding RNAs (cis-NATs).
Overexpression of BRI1_NAT resulted in 94 out of 97 transgenic Arabidopsis plants displaying a bri1 mutant-like dwarf phenotype.
Overexpression of CLV1_NAT resulted in 20 out of 39 transgenic Arabidopsis plants displaying abnormal club-shaped siliques and increased carpel number.
Overexpression of SOBIR1_NAT in Arabidopsis led to enhanced susceptibility to Pseudomonas syringae infection compared to wild-type plants.

Quotes

"Cis-NATs exhibit dynamic regulation with distinct expression patterns and therefore have the potential to fine-tune gene regulation in response to stimuli."
"For cis-NAT regulation to produce the specific expression patterns observed in LRR-RLKs, the cis-NATs must function cell autonomously."
"The association between LRR-RLKs and cis-NATs is not limited to Arabidopsis, but is conserved in diverse, agronomically important crops."

Key Insights Distilled From

Long non-coding RNAs regulate the expression of cell surface receptors in plants

by Mott,G. A., ... at www.biorxiv.org 04-22-2024

https://www.biorxiv.org/content/10.1101/2024.04.22.590565v1

Deeper Inquiries

How do the specific expression patterns and regulatory mechanisms of cis-NATs allow them to fine-tune the spatiotemporal expression of LRR-RLKs in response to different developmental and environmental cues?

Cis-NATs exhibit specific expression patterns that overlap with the expression of their cognate LRR-RLKs, allowing them to fine-tune the spatiotemporal expression of these receptors in response to various cues. The distinct expression patterns of cis-NATs, such as tissue-specific or inducible expression, enable them to regulate LRR-RLKs in a cell-autonomous manner. By being expressed in specific tissues or in response to particular stimuli, cis-NATs can modulate the expression of LRR-RLKs precisely where and when needed. This specificity ensures that the regulatory activity of cis-NATs is tightly controlled and targeted, contributing to the fine-tuning of LRR-RLK expression in different developmental stages and environmental conditions.
Furthermore, the regulatory mechanisms employed by cis-NATs, such as negative or positive regulation at the transcriptional, post-transcriptional, or translational levels, provide additional layers of control over LRR-RLK expression. For example, cis-NATs can negatively regulate LRR-RLK expression by interfering with transcription or mRNA stability, leading to downregulation of the receptor. Conversely, they can positively regulate LRR-RLK expression by enhancing translation or stabilizing the mRNA, resulting in increased receptor levels. This dynamic regulation by cis-NATs allows for precise adjustments in LRR-RLK expression levels in response to specific cues, ultimately fine-tuning plant growth, development, and immunity.

What are the potential applications of engineering cis-NAT regulation to improve agronomic traits in crop plants by modulating LRR-RLK function?

Engineering cis-NAT regulation presents exciting opportunities for improving agronomic traits in crop plants by modulating LRR-RLK function. By manipulating the expression and activity of cis-NATs associated with specific LRR-RLKs, researchers can potentially enhance desired traits in crops. Some potential applications include:

Enhanced stress tolerance: By overexpressing cis-NATs that positively regulate stress-responsive LRR-RLKs, crop plants can be engineered to exhibit improved tolerance to biotic and abiotic stresses. This could lead to increased crop yield and resilience in challenging environmental conditions.

Optimized growth and development: Modulating the expression of cis-NATs associated with growth-regulating LRR-RLKs can result in crops with enhanced growth characteristics, such as increased biomass, improved flowering time, and enhanced nutrient uptake. This could lead to improved crop productivity and quality.

Disease resistance: Manipulating the regulatory activity of cis-NATs that control immune-related LRR-RLKs can confer enhanced disease resistance in crop plants. By fine-tuning the expression of these receptors, crops can be engineered to better defend against pathogens and pests, reducing the need for chemical interventions.

Trait stacking: Engineering multiple cis-NAT-LRR-RLK regulatory modules in crop plants can enable the stacking of desirable traits, creating genetically modified crops with multiple beneficial characteristics. This approach could lead to the development of high-yielding, stress-tolerant, and disease-resistant crop varieties.

Overall, the precise control offered by cis-NAT regulation of LRR-RLKs provides a powerful tool for crop improvement, offering potential solutions to challenges in agriculture and contributing to sustainable and resilient crop production.

Given the conserved association between LRR-RLKs and cis-NATs, how did this regulatory mechanism evolve and what selective pressures drove its conservation across plant species?

The conserved association between LRR-RLKs and cis-NATs across plant species suggests an evolutionarily ancient and functionally important regulatory mechanism. Several factors likely contributed to the evolution and conservation of this regulatory system:

Functional significance: The critical roles played by LRR-RLKs in plant growth, development, and immunity would have exerted strong selective pressures to ensure precise and dynamic regulation of their expression. The association with cis-NATs may have evolved as an efficient mechanism to fine-tune LRR-RLK expression in response to diverse cues, contributing to plant fitness and adaptation.

Regulatory complexity: The combinatorial control of gene expression by cis-NATs, in addition to other regulatory elements like transcription factors, provides a higher level of regulatory complexity. This complexity enhances the robustness and adaptability of the regulatory network governing LRR-RLK expression, making it more resilient to genetic and environmental perturbations.

Conservation of function: The functional conservation of cis-NATs in regulating LRR-RLKs across plant species suggests that this regulatory mechanism confers evolutionary advantages. The shared association between LRR-RLKs and cis-NATs may have been maintained throughout plant evolution due to its effectiveness in modulating receptor expression and optimizing plant responses to changing environments.

Adaptive responses: The ability of cis-NATs to respond to specific developmental stages, tissues, or stress conditions allows for adaptive responses in plants. This flexibility in gene regulation likely provided a selective advantage, driving the conservation of the LRR-RLK-cis-NAT regulatory system across diverse plant species.

In conclusion, the evolution and conservation of the association between LRR-RLKs and cis-NATs reflect the importance of this regulatory mechanism in shaping plant development, adaptation, and survival. The selective pressures driving the conservation of this system highlight its functional significance and adaptive value in plant biology.