Feedback regulation of symbiotic N₂ fixation under drought stress

Abstract

-Although drought inhibition of N 2 fixation is general among rhizobium-legume symbioses, a large genetic variation has been found among legume species and cultivars in the N 2 fixation sensitivity to water deficits. Legume species that transport ureides from the nodules were found to be much more drought-sensitive than those that transport amides. It was concluded that a feedback mechanism involving ureide level may control N 2 fixation under drought. Consistent with this observation, the drought tolerance of N 2 fixation in soybean was associated with low concentrations of ureides in plant tissues. Experimental evidence for a direct inhibition of nitrogenase activity by ureides application supported the feedback hypothesis, although the exact nature of the chemical compound involved in the signal is still unknown. The basis for ureide accumulation is hypothesized to result from decreased ureide catabolism in the leaf. We showed recently that Asparagine (Asn) chelates Mn ions, which are the co-factor of the enzyme allantoate amidohydrolase, and as a result may cause an inhibition of ureide breakdown in the shoot. These data are consistent with the hypothesis that Asn would be a signal for the feedback inhibition of N 2 fixation. N 2 fixation / drought stress / feedback / ureides / soybean Résumé -Régulation « feedback » de la fixation symbiotique de N 2 sous déficit hydrique. Une large variabilité génétique a été mise en évidence parmi les espèces et cultivars de légumineuses pour la sensibilité de la fixation de N 2 au déficit hydrique. Les espèces de légumineuses qui transportent l'azote sous forme d'uréides se sont avérées plus sensibles que les espèces à amides. Il en a été déduit qu'un mécanisme de régulation de type « feedback » impliquant les uréides serait responsable de l'inhibition de la fixation de N 2 par déficit hydrique. Des résultats expérimentaux montrant une inhibition de l'activité nitrogénase par l'application d'uréides exogènes constituent une preuve supplémentaire en faveur de l'hypothèse de régulation « feedback ». Le mécanisme physiologique responsable de l'accumulation des uréides est supposé résulter d'une diminution du catabolisme foliaire des uréides, mais la nature exacte de la molécule chimique impliquée dans le signal reste encore inconnue. Nous avons montré récemment que l'asparagine (Asn) pourrait induire une inhibition de la dégradation des uréides dans les feuilles, et par conséquent, leur accumulation dans les différents tissus de la plante. Ces résultats soutiennent l'hypothèse de l'intervention de Asn comme signal de régulation du métabolisme des uréides et de la fixation symbiotique de N 2 sous déficit hydrique.

Medicago truncatulaRoot Nodule Proteome Analysis Reveals Differential Plant and Bacteroid Responses to Drought Stress

“…Water-deficit stress causes a well-documented decline in SNF in N 2 -fixing legumes (Arrese-Igor et al, 1999;Zahran, 1999;Serraj et al, 2001), which is also shown for nodulated M. truncatula plants in this study (Fig. 4B).…”

“…Under this stress, symbiotic nitrogen fixation (SNF) is one of the physiological processes to first show stress responses in nodulated legumes, occurring before the decrease in CO 2 -photosynthetic assimilation rates (Durand et al, 1987). Several hypotheses have been proposed by different research groups to explain the decline in nitrogen fixation during drought: (1) regulation through the control of carbon flux within nodules, mainly due to down-regulation of Suc synthase (SuSy; González et al, 1995;Gordon et al, 1997;ArreseIgor et al, 1999); (2) regulation based on the internal oxygen levels within nodules (Durand et al, 1987;Diaz del Castillo et al, 1994;Serraj and Sinclair, 1996); and (3) nitrogen feedback regulation (Serraj et al, 2001;King and Purcell, 2005). However, to date, the molecular mechanisms responsible for these physiological responses are not yet understood.…”

Nitrogen Fixation Control under Drought Stress. Localized or Systemic?

“…Systemic regulation of nitrogen fixation under environmental stress is believed to involve nitrogen feedback (Parsons et al, 1993;Parsons and Sunley, 2001;Serraj et al, 2001;King and Purcell, 2005), possibly operating through reduced oxygen permeability (Neo and Layzell, 1997). The potential for such regulation existed in this study as nitrogen circulation between split roots is widely accepted (Fisher, 2000) and has been shown for nodulated soybeans (Tanaka et al, 1985).…”

“…There is now evidence that signaling for BNF regulation can be provided by a nitrogen feedback mechanism involving shoot nitrogen status. Several molecules have been suggested to be involved in such a mechanism, including Gln (Neo and Layzell, 1997), ureides (Serraj et al, 2001), and Asn (Bacanamwo and Harper, 1997). More recently, King and Purcell (2005) suggested that a combination of ureide and Asp levels in nodules, plus the transport of several amino acids from leaves, might be involved in such a feedback inhibition mechanism in soybean (Glycine max).…”

Alfalfa and Its Symbiosis Responses to Osmotic Stress

“…Indeed, severe water deiciency disrupts the nitrogenase activity of the nodules by causing a rapid decrease in the supply of oxygen to the nodules and consequently an interruption of the adenosine triphosphate (ATP) supply to the nitrogenase [53]. It can also slowdown the transport of photosynthate towards the nodules, which limits the contribution of the energy substrates [54].…”