Non-coding RNAs in environmental adaptation

The non-coding transcriptome of two Arabidopsis ecotypes suggests new mechanisms for plant adaptation to soil environment

Protein-coding genes are largely conserved among organisms. This conservation is even stronger between ecotypes of the same species despite that these ecotypes can respond differently to the environment. The noncoding part of the genome is less conserved and may thus significantly contribute to this phenotypic variation such as a special category of RNAs that do not code for proteins: the noncoding RNAs (ncRNAs). As ncRNAs quantitatively regulate the expression of coding genes, they could be key novel players in the response to the environment. In plants, the root system development is very plastic and modifies its shape according to nutrient availability. For example, inorganic phosphate accumulates preferentially in the upper layer of the soil and, during phosphate starvation, certain plants stop their main root growth to develop lateral roots and explore the soil horizontally.

The team of Martin Crespi at the Institute of Plant Sciences Paris Saclay (IPS2, Paris-Saclay University), in collaboration with the groups of Thierry Desnos (UMR7265 SAVE, CEA-Cadarache) and of Daniel Gautheret (I2BC, Paris-Saclay University), investigated how ncRNAs may control ecotype adaptation to the environment (10.1104/pp.20.00446). They used two ecotypes of Arabidopsis thaliana that respond differentially to phosphate starvation: a) Columbia, which stops its main root growth and b) Landsberg erecta that continues to grow. For these two ecotypes, they analyzed in rootsfull transcriptome changes including coding genes, ncRNAs and small RNAs, after a short-term phosphate deprivation. Thousands of previously uncharacterized ncRNAs were identified whose encoding DNA is highly conserved between the two ecotypes. Despite this strong sequence conservation, half of the detected ncRNAs were transcribed in only one of the two ecotypes. In contrast, 90% of the protein-coding genes were expressed similarly in the two ecotypes during the phosphate starvation. Using plant mutants showing modified expression levels of five “ecotype-specific” ncRNAs, they could identify two new ncRNAs regulating primary root growth. One of these ncRNAs was linked to the regulation of genes involved in control of root growth and nutrient transport. Hence, by exploring Arabidopsis ecotype transcriptomes including ncRNAs, new regulatory mechanisms for plant root system adaptation to soil environment could be unraveled.

Figure legend: Above: Col-0 and Ler ecotypes respond differentially to phosphate starvation. Below: The transcriptomic difference between the two ecotypes or during phosphate starvation. While for the coding genes the number of differentially expressed genes between the ecotypes (3293) or during the phosphate starvation (2465) are of the same level of magnitude, the non-coding genes are clearly biased towards a differential ecotype regulation (672), including a hundred of ecotype “specific” ncRNAs (no expression in the other ecotype despite their DNA sequence conservation)..