Sorghum root epigenetic landscape during limiting phosphorus conditions

Authors: Gladman, Nicholas; HUFNAGEL, BARBARA - Centre National De La Recherche Scientifique; REGULSKI, MICHAEL - Cold Spring Harbor Laboratory; LIU, ZHIGANG - University Of Saskatchewan; WANG, XIAOFEI - Cold Spring Harbor Laboratory; CHOUGULE, KAPEEL - Cold Spring Harbor Laboratory; KOCHAIN, LEON - University Of Saskatchewan; MAGALHAES, JURANDIR - Embrapa; Ware, Doreen

Submitted to: Plant Direct
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/26/2022
Publication Date: 5/14/2022
Citation: Gladman, N.P., Hufnagel, B., Regulski, M., Liu, Z., Wang, X., Chougule, K., Kochian, L., Magalhaes, J., Ware, D. 2022. Sorghum root epigenetic landscape during limiting phosphorus conditions. Plant Direct. 6(5):e393. https://doi.org/10.1002/pld3.393.
DOI: https://doi.org/10.1002/pld3.393

Interpretive Summary: The root system of the globally important crop sorghum (Sorghum bicolor) undergoes distinct developmental changes during conditions where phosphorus is deficient in the soil, including the lateralization the roots closer to the topsoil. To understand the genetic and epigenetic alterations that underlie the observed physical changes, we have profiled the gene expression and epigenetic (DNA methylation and histone methylation) states of the sorghum cultivar BTx623 during limiting phosphorus conditions. These profiles have revealed that the lateral root sections undergo significantly more and larger gene expression changes during nutrient stress, and that the epigenetic modifications (methylations) occur predominately at regions of the genome that do not contain genes. Suggesting that the developmental changes that occur are resultant from a combination of epigenetic modifications that alter gene expression through manipulating the 'openness' of the chromatin surrounding genes. Additionally, we identified numerous sulfur and cysteine metabolism pathway genes that could play a role in proper root system response to limiting phosphorus. This revelation could lead towards additional targets of interest to optimize root systems for low-nutrient soil environments.

Technical Abstract: Efficient acquisition and use of available phosphorus from the soil is crucial for plant growth, development, and yield. With an ever-increasing acreage of croplands with suboptimal available soil phosphorus, genetic improvement of sorghum germplasm for enhanced phosphorus acquisition from soil is crucial to increasing agricultural output and reducing inputs, while confronted with a growing world population and uncertain climate. Sorghum bicolor is a globally important commodity for food, fodder, and forage. Known for robust tolerance to heat, drought, and other abiotic stresses, its capacity for optimal phosphorus use efficiency (PUE) is still being investigated for optimized root system architectures (RSA). Whilst a few RSA-influencing genes have been identified in sorghum and other grasses, the epigenetic impact on expression and tissue-specific activation of candidate PUE genes remains elusive. Here, we present transcriptomic, epigenetic, and regulatory network profiling of RSA modulation in the BTx623 sorghum background in response to limiting phosphorus (LP) conditions. We show that during LP, sorghum RSA is remodeled to increase root length and surface area, likely enhancing its ability to acquire P. Global DNA 5-methylcytosine and H3K4 and H3K27 trimethylation levels decrease in response to LP, while H3K4me3 peaks and DNA hypomethylated regions contain recognition motifs of numerous developmental and nutrient responsive transcription factors that display disparate expression patterns between different root tissues (primary root apex, elongation zone, and lateral root apex). Suggesting that epigenetic shifts during growth on LP results in targeted gene expression in a tissue-specific manner that optimizes the RSA for improved P uptake.