Transcriptional reprogramming and co-expression network underlying enhanced ammonium uptake in intraspecific hybrids of Saccharum spontaneum

TL;DR

This study explores how intraspecific hybrids of Saccharum spontaneum improve ammonium uptake through transcriptional changes and gene networks.

Contribution

The paper reveals a novel regulatory network and transcriptional reprogramming in hybrids that enhance nitrogen use efficiency.

Findings

Hybrids showed enhanced ammonium uptake but not nitrate uptake.

Transcriptional reprogramming involved downregulation of nitrate assimilation genes and rewiring of carbon metabolism.

Fourteen core genes were identified as part of a regulatory network linked to ammonium uptake.

Abstract

In sugarcane production, nitrogen utilization efficiency is generally suboptimal, averaging only 30–40%. Saccharum spontaneum, the wild progenitor of sugarcane, harbors abundant genetic resources for high nitrogen efficiency, which remain largely untapped. Notably, the application of intraspecific hybridization in S. spontaneum for improving nitrogen efficiency in sugarcane breeding remains unexplored.

Against this background, in March 2024, an initial investigation was conducted at the Sugarcane Research Institute of the Yunnan Academy of Agricultural Sciences, China, focusing on four S. spontaneum germplasm materials (YN82, GSM22, GSM12, YN2) and two intraspecific F1 hybrids (A2, B1), to explore the mechanisms underlying heterosis in nitrogen use efficiency in S. spontaneum.

Physiological assays revealed that the hybrids specifically enhanced ammonium (15NH4+) uptake capacity but not nitrate uptake. Comparative transcriptomics and weighted gene co-expression network analysis (WGCNA) unveiled a systemic transcriptional reprogramming in hybrids. This reprogramming involved the coordinated downregulation of nitrate assimilation genes and the rewiring of starch/sucrose metabolism, facilitating carbon skeleton supply for energetically favorable ammonium assimilation. WGCNA identified key modules significantly correlated with ammonium uptake. From these modules, we pinpointed 14 core candidate genes constituting a multi-layered regulatory network, encompassing transcription factors (e.g., AP2/EREBP, bHLH, MYB), nitrogen assimilation enzymes (GAD), carbon metabolism providers (TPP, TPS), and root development regulators (HCT, CYP84A1).

Our work deciphers how intraspecific hybridization triggers systemic optimization to improve NUE and provides novel gene resources for breeding nitrogen-efficient sugarcane.

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