Root exudates drive interspecific facilitation by enhancing nodulation and N ₂ fixation

Abstract

Plant diversity in experimental systems often enhances ecosystem productivity, but the mechanisms causing this overyielding are only partly understood. Intercropping faba beans (Vicia faba L.) and maize (Zea mays L.) result in overyielding and also, enhanced nodulation by faba beans. By using permeable and impermeable root barriers in a 2-y field experiment, we show that root-root interactions between faba bean and maize significantly increase both nodulation and symbiotic N 2 fixation in intercropped faba bean. Furthermore, root exudates from maize promote faba bean nodulation, whereas root exudates from wheat and barley do not. Thus, a decline of soil nitrate concentrations caused by intercropped cereals is not the sole mechanism for maize promoting faba bean nodulation. Intercropped maize also caused a twofold increase in exudation of flavonoids (signaling compounds for rhizobia) in the systems. Roots of faba bean treated with maize root exudates exhibited an immediate 11-fold increase in the expression of chalcone-flavanone isomerase (involved in flavonoid synthesis) gene together with a significantly increased expression of genes mediating nodulation and auxin response. After 35 d, faba beans treated with maize root exudate continued to show up-regulation of key nodulation genes, such as early nodulin 93 (ENOD93), and promoted nitrogen fixation. Our results reveal a mechanism for how intercropped maize promotes nitrogen fixation of faba bean, where maize root exudates promote flavonoid synthesis in faba bean, increase nodulation, and stimulate nitrogen fixation after enhanced gene expression. These results indicate facilitative root-root interactions and provide a mechanism for a positive relationship between species diversity and ecosystem productivity.flavanoids | gene expression | intercropping | root-root interactions | signals M any ecosystems, including grasslands (1, 2), forests (3), phytoplankton communities (4), and cropping systems (5), show a positive relationship between plant diversity and ecosystem productivity. Several mechanisms have been proposed to explain this relationship. A "sampling effect" occurs, because more diverse mixtures have a higher probability of containing a species with higher productivity (6). Complementarity effects occur when species vary in resource use and niche differentiation in space or time, leading to greater resource utilization (6-9). Facilitation occurs when one species increases the growth of other species through a wide range of processes (10). Facilitative effects may be direct (e.g., by shade or protection from harsh conditions) or indirect (e.g., when one species reduces attack by pathogens or herbivores on other species) (11-13).Legume/cereal intercropping systems have been widely studied in the context of diversity and ecosystem function and commonly overyield, because dinitrogen (N 2 ) fixation by legumes increases ecosystem nitrogen (N) supply (7,8), an example of facilitation. This facilitation is important to agriculture on a large scale, because app...

Advances in the rhizosphere: stretching the interface of life

“…intercropping systems (Li et al 2007(Li et al , 2014. Positive plant-plant interactions, such as root-root facilitation, have been shown to play a significant role for P acquisition (Li et al 2007;Brooker et al 2015;Li et al 2016;Zhang et al 2016). Tang et al (2016) further demonstrated the greater performance of such intercropping systems compared to single crop systems under field conditions along a P fertility gradient.…”

“…Through their nutritive effects, exudates will affect the structure of soil microbial communities, favoring cell division of bacteria able to catabolize them. Though microbe-plant chemical dialogues are well-known in the case of symbiotic interactions between legumes and nitrogen-fixing rhizobia (Limpens et al 2015;Li et al 2016) or in plant mycorrhiza (Parniske 2008), these are less well characterized in plant-PGPR interactions.…”

“…However, this is not a unidirectional path as the root microbiome also produces many metabolites and thus also able to affect the composition of the chemical cocktail in the rhizosphere.. These mutual interactions ultimately affect nutrient availability for all partners (Lambers et al 2008), plant health (Berendsen et al 2012) and root-root interactions (Semchenko et al 2014), cascading into ecosystem functions such as productivity (Latz et al 2012;Li et al 2016) and soil formation (Lambers et al 2009;Keiluweit et al 2015;Lange et al 2015). The challenge now is to reveal the functionality of these multifacetted interactions between plant roots, root exudates, microbial metabolites, the root microbiome and the soil..Management of this multicomponent complexity of the rhizosphere and its relationship to soil fertility will become crucial in order to maintain food production with reduced fertiliser and pesticide inputs .…”

Identification and Functional Characterization an Ortholog of OsENOD93-1 Gene in Wheat Using in-silico Approach

“…These genes play a critical role in different biological processes associated with NUE such as uptake, assimilation, and utilization efficiency (Han et al, 2016). Early nodulation 93 (ENOD93) gene play a significant role in cell wall reorganization during nodulation in legumes (Li et al, 2016). ENOD93 is an active member of early nodulin-like proteins family.…”

“…Overexpression of OsENOD93-1 in transgenic rice plant increased the shoot dry biomass and seed yield. Li et al, (2016) suggested that ENOD93 gene showed up-regulation and promoted nitrogen fixation in faba beans. Despite the critical interplay of ENOD93-1 gene in N regulation, no efforts were made in past to identify ENOD93-1 gene in wheat.…”