A miR169c-NFYA10 module confers tolerance to low-nitrogen stress to Betula luminifera

Abstract

Betula species constitute a large portion of species in forest ecosystems, are a key player in biomass resources and are recognized as pioneer species with strong stress tolerance. The miR169-NFYA module plays essential roles in the response to abiotic stress, including nutrient stress. However, the functional roles of the miR169-NFYA module in Betula luminifera, an important subtropical and pioneer forestry tree species, in response to nitrogen (N) starvation are not well documented. In the present study, ten BlNFYA genes were identified in B. luminifera. The expression of most BlNFYAs increased under low-nitrogen (LN) stress, while the expression of BlmiR169 was inhibited; among them, BlmiR169c and its corresponding target gene BlNFYA10 might play important regulatory roles in response to N availability. We then functionally investigated BlmiR169c-BlNFYA10 in response to LN stress and determined its regulatory roles in response to N starvation by analyzing the expression patterns, miRNA-mRNA interactions, phenotypes, and physiological and transcriptomic responses of transgenic Arabidopsis and birch roots under LN stress. Overexpression of BlmiR169c and BlNFYA10 resulted in contrasting tolerance to N starvation, and BlNFYA10 provided transgenic plants with LN tolerance with lower growth costs compared with those of the wild type under LN stress. This tolerance might involve a trade-off between growth and defense by upregulating defense- and downregulating photosynthesis- and translation-related activities under LN stress. On the other hand, BlNFYA10 provided transgenic plants with enhanced uptake and assimilation of N, effectively compensating for the defense-growth trade-offs in BlNFYA10-overexpressing plants. Our data demonstrate that a potential regulatory mechanism of BlmiR169c-BlNFYA10 is involved in the LN stress response, providing a basis for increasing the nitrogen-use efficiency (NUE) of B. luminifera and/or other forestry tree species.