An ABA/auxin regulatory module controlled by nitrogen governs symbiotic organogenesis in the bryophyte species Ricciocarpos natans

Abstract

During the terrestrialization of plants c. 470 Ma, overcoming nitrogen limitation was a major evolutionary challenge. While nonvascular plants may acquire nitrogen through rhizoids and surface diffusion, symbiotic interactions likely provide an important strategy to overcome nitrogen limitation. This study reveals that the amphibious liverwort Ricciocarpos natans (an extant bryophyte lineage) undergoes nitrogen‐driven organogenesis. Under nitrogen‐limiting conditions, the plant reprograms its development to form specialized scales, creating symbiotic niches. The formation of these symbiotic scales is activated by a nitrogen‐sensing mechanism that suppresses the abscisic acid (ABA) and auxin signaling pathways. This hormonal reprogramming promotes an aquatic morphology with robust scales while suppressing the terrestrial form. These specialized scales likely support colonization by nitrogen‐fixing bacteria, exemplified here using the model diazotroph Rhodopseudomonas palustris, demonstrating the capacity of ventral scales to function as symbiotic niches that enhance host nitrogen acquisition. This discovery identifies a nitrogen‐responsive, scale‐associated symbiotic strategy in Ricciocarpos natans (Marchantiales), providing comparative insight into how nonvascular plants adapt to nitrogen limitation and offering mechanistic clues regarding microbial recruitment pathways in plant–microbe interactions.