Bradyrhizobial invasion in dalbergoid legumes like Arachis hypogaea and endophytic bacterial invasions in non-legumes like Oryza sativa occur through epidermal cracks. Here, we show that there is no overlap between the bradyrhizobial consortia that endosymbiotically and endophytically colonise these plants. To minimise contrast due to phylogeographic isolation, strains were collected from Arachis/Oryza intercropped fields and a total of 17 bradyrhizobia from Arachis (WBAH) and 13 from Oryza (WBOS) were investigated. 16SrRNA and concatenated dnaK-glnII-recA phylogeny clustered the nodABC-positive WBAH and nodABC-deficient WBOS strains in two distinct clades. The in-field segregation is reproducible under controlled conditions which limits the factors that influence their competitive exclusion. While WBAH renodulated Arachis successfully, WBOS nodulated in an inefficient manner. Thus, Arachis, like other Aeschynomene legumes support nod-independent symbiosis that was ineffectual in natural fields. In Oryza, WBOS recolonised endophytically and promoted its growth. WBAH however caused severe chlorosis that was completely overcome when coinfected with WBOS. This explains the exclusive recovery of WBOS in Oryza in natural fields and suggests Nod-factors to have a role in counterselection of WBAH. Finally, canonical soxY1 and thiosulphate oxidation could only be detected in WBOS indicating loss of metabolic traits in WBAH with adaptation of symbiotic lifestyle.
The lncRNA ENOD40 is required for cortical cell division during root nodule symbiosis (RNS) of legumes, though it is not essential for actinorhizal RNS. Our objective was to understand whether ENOD40 was required for aeschynomenoid nodule formation in Arachis hypogaea. AhENOD40 express from chr5 (AhENOD40-1) and chr15 (AhENOD40-2) during symbiosis, and RNA interference of these transcripts drastically affected nodulation indicating the importance of ENOD40 in A.hypogaea. Furthermore, we demonstrated several distinct characteristics of ENOD40: (i) Natural antisense transcript of ENOD40 was detected from the AhENOD40-1 locus (designated as NAT-AhDONE40). (ii) Both AhENOD40-1 and AhENOD40-2 had two exons, whereas NAT-AhDONE40 was monoexonic. RT-qPCR analysis indicated both sense and antisense transcripts to be present in both cytoplasm and nucleus, and their expression increased with the progress of symbiosis. (iii) RNA Pulldown from whole cell extracts of infected roots at 4DPI indicated NAT-AhDONE40 to interact with the SET (Su(var)3-9, Enhancer-of-zeste and Trithorax) domain containing Ash (Absent Small homeotic disc) family protein AhASHR3 and this interaction was further validated using RNA immunoprecipitation and EMSA. (iv) ChIP assays indicate deposition of ASHR3 specific histone marks H3K36me3 and H3K4me3 in both the ENOD40 loci during the progress of symbiosis. ASHR3 is known for its role in optimizing cell proliferation and reprogramming. Since both ASHR3 and ENOD40 from legumes cluster away from those in actinorhizal plants and other nonlegumes in phylogenetic distance trees, we hypothesize that the interaction of DONE40 with ASHR3 could have evolved for adapting the nodule organogenesis program for legumes.
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