Host Genotype Shapes Fungal Symbiont-Mediated Nutrient and Growth Benefits in Citrus

Given the global economic importance of citrus and growing threats from climate change and soil degradation, this study investigated how arbuscular mycorrhizal (AM) fungi (Funneliformis mosseae, Fm, formerly Glomus mosseae; Diversispora versiformis, Dv, formerly Glomus versiforme) and endophytic fungus Serendipita indica (Si, formerly Piriformospora indica) differentially enhance spring shoot growth, nutrient acquisition, phytohormone profiles, and expression patterns of Fe/Mg transporter genes in two citrus cultivars (‘Beni-Madonna’ and ‘Lane Late’). Si achieved higher root colonization than AM fungi (Fm/Dv) in both cultivars, with peak colonization observed in September. Fungal inoculation differentially enhanced spring shoot growth and leaf gas exchange, with Fm and Dv demonstrating cultivar-specific effects, while Si consistently increased shoot number across cultivars but showed limited gas exchange influence in ‘Lane Late’. In ‘Beni-Madonna’, AM fungi broadly enhanced auxins/cytokinins, while Si specifically increased indole-3-acetic acid and dihydrozeatin but reduced N6-isopentenyladenine; ‘Lane Late’ showed comprehensive hormone upregulation by all fungi except Si’s dihydrozeatin suppression. AM fungi enhanced Ca, Mg, and Mn in ‘Beni-Madonna’ and P, S, Zn, and B in ‘Lane Late’, while Si increased Fe and Zn in the former and P, S, and B in the latter. Fungal symbionts differentially regulated Fe/Mg transporter genes in a cultivar-specific manner. In ‘Beni-Madonna’, Fm upregulated key Fe transporters (CsFRO1, CsHA1, and CsIRT1) while Si broadly enhanced all Fe transporters, correlating with increased leaf Fe levels; Fm specifically induced CsMGT2 and CsMGT8, showing strong association with Mg accumulation. ‘Lane Late’ exhibited distinct responses, with Si comprehensively activating both Fe (CsFRO1, CsHA1-2, and CsIRT1-2) and Mg (CsMGT6/8) transporter genes, while Dv showing minimal effects. These findings demonstrate that fungal symbionts differentially regulate citrus growth and nutrient homeostasis in a cultivar-dependent manner, highlighting the importance of host genotype-specific fungal partnerships for sustainable citrus production.