Global integrators of light signalling and nutrient homeostasis safeguard symbiosis under light stress

Their large, protein-rich seeds render many legume plants like beans, peas or soy attractive food or fodder crops. This is thanks to nitrogen-fixing root nodulation symbiosis (RNS) with rhizobial bacteria, a mutualistic association enabling legumes to not only form storage seeds, but also thrive in nitrogen poor habitats. These benefits come at a cost: accommodating millions of bacteria that actively fix N2 requires substantial nutrient and energy input. Evolutionarily successful hosts employ a multi-layered regulatory system balancing endogenous nutrient status and interorganismal nutrient exchange with symbiosis establishment and progression. Root infection as well as nodule organogenesis and -lifespan are tightly regulated, ensuring a mutualistic status. Under adverse conditions, established nodules can be deactivated by induction of nodule senescence in a process involving the transcription factor genes NAM ATAF CUC (NAC) 094 (Wang et al., 2023) and FIXATION UNDER NITRATE (FUN) (Lin et al., 2024). The molecular basis and role of senescence induction in RNS regulation is still far from understood. Here, we demonstrate that in Lotus japonicus, the two photomorphogenesis genes ELONGATED HYPOCOTYL5 (HY5) and the B-Box-containing zinc finger transcription factor gene BBX21 are required and sufficient for maintaining nodule function under high light intensities. Loss of either HY5 or BBX21 results in a light-dependent increase of NAC094 transcript levels, nodule necrosis and early senescence, and enhanced nodule proliferation. Moreover, expression of dominant negative HY5 or BBX21 is sufficient to induce nodule necrosis and hypernodulation. Our data establish LjHY5 and LjBBX21 as a novel gene pair safeguarding nodule function and nitrogen fixation by preventing light induced senescence. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=114 SRC="FIGDIR/small/741514v1_ufig1.gif" ALT="Figure 1"> View larger version (22K): org.highwire.dtl.DTLVardef@3b06dforg.highwire.dtl.DTLVardef@1403f85org.highwire.dtl.DTLVardef@10a42bdorg.highwire.dtl.DTLVardef@a3921c_HPS_FORMAT_FIGEXP M_FIG Graphical abstract C_FIG