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Mucoromycotina is one of the earliest fungi to establish a mutualistic relationship with plants in the ancient land. However, the detailed information on their carbon supply from the host plants is largely unknown. In this research, a free-living Mucoromycotina called  Gongronella  sp. w5 (w5) was employed to explore its effect on  Medicago truncatula  growth and carbon source utilization from its host plant during the interaction process. W5 promoted  M. truncatula  growth and caused the sucrose accumulation in  M. truncatula  root tissue at 16 days post-inoculation (dpi). The transportation of photosynthetic product sucrose to the rhizosphere by  M. truncatula  root cells seemed accelerated by upregulating the SWEET gene. A predicted cytoplasmic invertase ( GspInv ) gene and a sucrose transporter ( GspSUT1 ) homology gene in the w5 genome upregulated significantly at the transcriptional level during w5– M. truncatula  interaction at 16 dpi, indicating the possibility of utilizing plant sucrose directly by w5 as the carbon source. Further investigation showed that the purified GspInv displayed an optimal pH of 5.0 and a specific activity of 3380 ± 26 U/mg toward sucrose. The heterologous expression of  GspInv  and  GspSUT1  in  Saccharomyces cerevisiae  confirmed the function of GspInv as invertase and GspSUT1 as sugar transporter with high affinity to sucrose  in vivo . Phylogenetic tree analysis showed that the ability of Mucoromycotina to utilize sucrose from its host plant underwent a process of “loss and gain.” These results demonstrated the capacity of Mucoromycotina to interact with extant land higher plants and may employ a novel strategy of directly up-taking and assimilating sucrose from the host plant during the interaction.

Mucoromycotina Fungi Possess the Ability to Utilize Plant Sucrose as a Carbon Source: Evidence From Gongronella sp. w5