Comparative transcriptome analysis of nodules of two Mesorhizobium–chickpea associations with differential symbiotic efficiency under phosphate deficiency

Abstract

Phosphate (Pi) deficiency is known to be a major limitation for symbiotic nitrogen fixation (SNF), and hence legume crop productivity globally. However, very little information is available on the adaptive mechanisms, particularly in the important legume crop chickpea (Cicer arietinum L.), which enable nodules to respond to low-Pi availability. Thus, to elucidate these mechanisms in chickpea nodules at molecular level, we used an RNA sequencing approach to investigate transcriptomes of the nodules in Mesorhizobium mediterraneum SWRI9-(MmSWRI9)-chickpea and M. ciceri CP-31-(McCP-31)-chickpea associations under Pi-sufficient and Pi-deficient conditions, of which the McCP-31-chickpea association has a better SNF capacity than the MmSWRI9-chickpea association during Pi starvation. Our investigation revealed that more genes showed altered expression patterns in MmSWRI9-induced nodules than in McCP-31-induced nodules (540 vs. 225) under Pi deficiency, suggesting that the Pi-starvation-more-sensitive MmSWRI9-induced nodules required expression change in a larger number of genes to cope with low-Pi stress than the Pi-starvation-less-sensitive McCP-31-induced nodules. The functional classification of differentially expressed genes (DEGs) was examined to gain an understanding of how chickpea nodules respond to Pi starvation, caused by soil Pi deficiency. As a result, more DEGs involved in nodulation, detoxification, nutrient/ion transport, transcriptional factors, key metabolic pathways, Pi remobilization and signalling were found in Pi-starved MmSWRI9-induced nodules than in Pi-starved McCP-31-induced nodules. Our findings have enabled the identification of molecular processes that play important roles in the acclimation of nodules to Pi deficiency, ultimately leading to the development of Pi-efficient chickpea symbiotic associations suitable for Pi-deficient soils.

Legume genetic resources and transcriptome dynamics under abiotic stress conditions

“…In addition to the above abiotic stressors, Pi deficiency is known to be a major limitation for symbiotic N 2 fixation, and hence can reduce legume crop productivity (Kleinert, Thuynsma, Magadlela, Benedito, & Valentine, ; Nasr Esfahani et al, ). Recently, Nasr Esfahani et al () investigated transcriptome changes in the nodules of Mesorhizobium ciceri CP‐31‐( Mc CP‐31)‐chickpea and Mesorhizobium mediterraneum SWRI9‐( Mm SWRI9)‐chickpea associations under Pi‐deficient and Pi‐sufficient conditions.…”

“…In addition to the above abiotic stressors, Pi deficiency is known to be a major limitation for symbiotic N 2 fixation, and hence can reduce legume crop productivity (Kleinert, Thuynsma, Magadlela, Benedito, & Valentine, ; Nasr Esfahani et al, ). Recently, Nasr Esfahani et al () investigated transcriptome changes in the nodules of Mesorhizobium ciceri CP‐31‐( Mc CP‐31)‐chickpea and Mesorhizobium mediterraneum SWRI9‐( Mm SWRI9)‐chickpea associations under Pi‐deficient and Pi‐sufficient conditions. Transcriptome analysis showed that Pi deficiency caused changes in the expression of more genes in Pi‐deficiency‐more‐sensitive Mm SWRI9‐induced nodules than in Pi‐deficiency‐less‐sensitive Mc CP‐31‐induced nodules, demonstrating distinct changes in gene expression in the two Mesorhizobium species in response to Pi deficiency (Nasr Esfahani et al, ).…”

“…NGS technologies have now been applied to many important crop plants to help understand the genetics of complex traits, and to provide insight into genomic variations, such as single nucleotide polymorphisms (SNPs), insertions/deletions, and other structural of variances (O'Rourke, Bolon, Bucciarelli, & Vance, ; Valliyodan et al, ; Yuan, Bayer, Batley, & Edwards, ). These advanced technologies have also facilitated the development of gene expression atlases and increased our understanding of the signalling pathways involved in the responses of plants to environmental stresses (Abdelrahman et al, ; Abdelrahman, Suzumura, et al, ; Abdelrahman, El‐Sayed, Sato, et al, ; Bhattacharjee, Ghangal, Garg, & Jain, ; Nasr Esfahani et al, ; Zhang, Chu, & Zhang, ). However, during domestication, the genomes of many crop species have changed relative to that of their wild progenitors, with increasing numbers of repetitive DNA sequences that can lead to incomplete or misassembled regions when NGS is used for sequencing, as NGS‐read lengths are too short to adequately cover these repeats (Abdelrahman, Suzumura, et al, ; Flint‐Garcia, ; Pavlovich, ; Yuan et al, ).…”

“…In addition, a shift in cultivated land use toward legume production can potentially lower the carbon footprint for the production of proteins needed for human consumption, increase N use efficiency, and enhance soil fertility (Considine et al, ; Foyer et al, ; Song et al, ; Sosa‐Valencia et al, ). However, the sustainability of legume crop production is threatened by the increasing incidence of environmental stresses, including persistent drought, increasing soil salinity, heat waves, and soil nutritional deficiencies (Aranjuelo, Cabrerizo, Aparicio‐Tejo, & Arrese‐Igor, ; Kunert et al, ; Maqbool, Aslam, & Ali, ; Nasr Esfahani et al, ; Valdés‐López et al, ; Zhang et al, ). For these reasons, it is essential to intensify legume genetic enrichment programmes, by using advanced breeding approaches and techniques, to develop legume cultivars that possess genetic resilience to environmental stresses.…”

“…In the last 5 years, rapid advances have been made in genome sequencing of many legume crops, including soybean, Lotus japonicus , Medicago truncatula , pigeon pea, and chickpea (Garg et al, ; Jain et al, ; Song et al, ; Valdés‐López et al, ; Varshney et al, ). This has also advanced legume transcriptomics, and SNP and gene discovery for various traits important for the productivity of legumes under both normal and stressful environmental conditions (Garg et al, ; Garg, Singh, Rajkumar, Kumar, & Jain, ; Ha et al, ; Nasr Esfahani et al, ; Patil et al, ; Valliyodan et al, ). Despite these advances, the programmes developing stress‐resistant legume cultivars still lag behind those of cereals, and the gradual increase in legume production over the past decade has been attributed to the increases in the area planted rather than to the development of new or genetically improved cultivars with greater yield potentials (Figure ; Anderson, Kono, Stupar, Kantar, & Morrell, ; Considine et al, ; Foyer et al, ).…”