Pea nodule gradients explain C nutrition and depressed growth phenotype of hypernodulating mutants

Abstract

Legumes are major plants for sustainable agriculture because legumes fix atmospheric N2 in symbiosis with soil bacteria. Previous investigations have attempted to increase N2 fixation by creating hypernodulating mutants for several legume species. However, such genetic mutation has failed to increase symbiotic fixation because hypernodulation is usually associated with depressed plant growth. Such failure is due to our lack of knowledge on the mechanisms of carbon flow. In particular, the impact of hypernodulation on carbon uptake and partitioning between the shoot, roots and nodules has never been quantified. Here we grew two wild pea genotypes and nine hypernodulating pea mutants in hydroponics. Measurements were made at the end of the vegetative period. We counted the nodules: for pea mutants, nodule number ranged from 500 to 2,600 per plant using genetic and allele strength variation. For pea wild types, nodule number ranged from 184 to 955 per plant, using environmental manipulation. We also measured carbon nutrition traits such as leaf area, radiation use efficiency for biomass production and biomass partitioning among shoot, roots and nodules. Relationships between nodule number and traits were analysed within hypernodulating mutants. Those relationships were then compared to those obtained for wild types. Our results show that total nodule biomass increases with nodule number for hypernodulating mutants and wild types. Mean nodule size decreases with nodule number for hypernodulating mutants and wild types. For mutants, root growth was reduced from 60 % for the lower hypernodulating to 80 % for the higher hypernodulating, compared to wild types. For mutants, shoot growth was reduced from 0 % for the lower hypernodulating to 60 % for the higher hypernodulating, compared to wild types. Evidence for decreased C uptake capacity is shown by 50 % less leaf area and 18 % less radiation use efficiency of the higher hypernodulating phenotypes. This is the first whole plant comparative study of hypernodulating mutants and wild types revealing relationships between carbon nutrition and nodule gradients. Our findings reveal some mechanisms that account for the depressed growth phenotype associated with hypernodulation in pea.