Transcription factor MdHB52 mediates phosphorus uptake by regulating methyl jasmonate secretion in apple rootstock

Phosphorus (P) deficiency is a prevalent constraint in agricultural soils, which limiting plant growth and productivity. In apple (Malus domestica Borkh.), the molecular mechanisms underlying the response to low-P (LP) stress remain largely unclear. Here, we employed a multi-omics approach to elucidate the mechanism of apple rootstock response to low-P stress. The progenies derived from LP-tolerant (PT) apple rootstock Baleng Crab (Malus robusta Rehd., BC) × LP-sensitive (PS) rootstock M9 (M. pumila Mill.) were used for bulked segregant analysis sequencing (BSA-seq) and RNA-sequencing. Integrating variation information, transcript levels and function annotation, 24 candidate genes related to low-P tolerance were predicted from the quantitative trait locus (QTL) regions. Furthermore, metabolomic profiling of parental root exudates revealed significantly higher methyl jasmonate (MeJA) secretion in BC under LP stress compared with that in M9. The association analysis demonstrated a negative relationship between the expression of HOMEOBOX PROTEIN 52 (MdHB52) from the candidate genes and MeJA biosynthetic genes. Silencing MdHB52 resulted in increased MeJA secretion and elevated P content. MdHB52 bound to the promoters of MeJA biosynthetic genes and suppressed their expression. Interestingly, a single nucleotide polymorphism variation within the MdHB52 promoter of the PT apple rootstocks disrupted the MYBCORE cis element, affecting its expression level and leading to increased MeJA secretion and P uptake. This study identified reliable candidate genes through multi-omics analysis, providing valuable insights for apple rootstock breeding aimed at enhancing tolerance to P-deficient soils.