Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes

Abstract

Access to fixed or available forms of nitrogen limits the productivity of crop plants and thus food production. Nitrogenous fertilizer production currently represents a significant expense for the efficient growth of various crops in the developed world. There are significant potential gains to be had from reducing dependence on nitrogenous fertilizers in agriculture in the developed world and in developing countries, and there is significant interest in research on biological nitrogen fixation and prospects for increasing its importance in an agricultural setting. Biological nitrogen fixation is the conversion of atmospheric N2 to NH3, a form that can be used by plants. However, the process is restricted to bacteria and archaea and does not occur in eukaryotes. Symbiotic nitrogen fixation is part of a mutualistic relationship in which plants provide a niche and fixed carbon to bacteria in exchange for fixed nitrogen. This process is restricted mainly to legumes in agricultural systems, and there is considerable interest in exploring whether similar symbioses can be developed in nonlegumes, which produce the bulk of human food. We are at a juncture at which the fundamental understanding of biological nitrogen fixation has matured to a level that we can think about engineering symbiotic relationships using synthetic biology approaches. This minireview highlights the fundamental advances in our understanding of biological nitrogen fixation in the context of a blueprint for expanding symbiotic nitrogen fixation to a greater diversity of crop plants through synthetic biology.

Medicago truncatula copper transporter 1 (MtCOPT1) delivers copper for symbiotic nitrogen fixation

“…Symbiotic nitrogen fixation relies heavily on a number of metalloproteins to carry out such a complex and energetically costly reaction (Brear et al ., ; González‐Guerrero et al ., , ). Therefore, studying how metals are allocated from the host plant to the nitrogen‐fixing rhizobia is of great importance in view of renewed efforts to engineer nitrogen fixation capabilities in nonlegumes (Oldroyd & Dixon, ; Ivleva et al ., ; Lopez‐Torrejon et al ., ; Mus et al ., ). In this context, a substantial effort has been dedicated to studying how iron (Fe) is delivered to the nodule and released into the apoplast (Rodríguez‐Haas et al ., ), a process likely facilitated by citrate (Takanashi et al ., ), to identify the plant transporters involved in Fe transport in rhizobia‐infected cells (Kaiser et al ., ; Hakoyama et al ., ; Tejada‐Jiménez et al ., ), and to describing mechanisms of Fe buffering in the bacteroid (Zielazinski et al ., ).…”

Rooting for cassava: insights into photosynthesis and associated physiology as a route to improve yield potential

“…However, as plant genomes and partial genomes have been revealed, it has become apparent that much of the signaling pathway required for nodulation, including that required for mycorrhiza formation, is probably present in all flowering plants. Although best known in leguminous plants ( Fabales ), N‐fixing bacteria in nodules have also evolved in the Rosales , Fagales and Cucurbitales , which suggests that engineering this into other dicots may be less of a challenge than previously envisaged (Delaux et al ., 2015a; Mus et al ., ). Indeed, it appears that the ancestor of land plants was already adapted to this symbiosis, such that their descendants may be predisposed for symbiosis with N‐fixing microbes (Delaux et al ., 2015b).…”

Crops, Nitrogen, Water: Are Legumes Friend, Foe, or Misunderstood Ally?

“…Other reviews focus on the bacterial and actinorhizal aspects of BNF under global change [17], BNF in non-legumes [18], and optimizing BNF via coordinated development and metabolism of legume host and rhizobial symbiont [19]. A comprehensive overview of the evolution of BNF and efforts to 'engineer' symbiotic relationships between organisms capable of BNF and host plants is given in [20][21][22][23]. The authors of [24] explored links between plant N and phosphorous (P) status and the persistence of BNF by legumes.…”