Synthesis, function, and genetic variation of sorgoleone, the major biological nitrification inhibitor in sorghum

Abstract

Sorghum is the third most important food crop, grown on nearly 40 million ha globally, and is known for its resilience under unfavorable conditions. Sorghum is reported to have a strong biological nitrification inhibition (BNI) capacity in root systems, a plant function that suppresses soil nitrifier activity, which in turn prevents the nitrogen (N) loss by reducing nitrous oxide (N₂O), nitric oxide (NO) emission, and nitrate (NO₃⁻) leaching into water bodies. Sorgoleone, a major hydrophobic phytochemical released from sorghum roots, provides a significant part of BNI function in sorghum. The function of sorgoleone in suppressing nitrifying bacteria in pure cultures has been established. In addition, sorgoleone suppresses transformation of ammonium (NH₃) to NO₃⁻ and N₂O emissions from soils. Therefore, introducing high-sorgoleone phenotype into elite sorghum hybrids can increase nitrogen use efficiency while decreasing the environmental footprint of sorghum production systems. In recent years, significant progress has been made in identifying the mechanisms of sorgoleone production and secretion. Moreover, studies using both wild accessions and elite breeding materials reported significant genetic variation for sorgoleone secretion, and sorgoleone secretion was found to be highly heritable, making it a good target for breeding. This review distills the current understanding of sorgoleone release in relation to BNI function and opportunities to exploit this trait. Also, we provide our assessment for genetic interventions of Sorgoleone biosynthesis and secretion pathways to enhance BNI capacity in sorghum. High-BNI sorghum hybrids can be an important component of low-nitrifying, low-N₂O-emitting agricultural production systems that are eco-friendly, productive, and sustainable.