Endoreduplication-mediated initiation of symbiotic organ development in Lotus japonicus

Abstract

Many leguminous plants have a unique ability to reset and alter the fate of differentiated root cortical cells to form new organs of nitrogenfixing root nodules during legume-Rhizobium symbiosis. Recent genetic studies on the role of cytokinin signaling reveal that activation of cytokinin signaling is crucial to the nodule organogenesis process. However, the genetic mechanism underlying the initiation of nodule organogenesis is poorly understood due to the low number of genes that have been identified. Here, we have identified a novel nodulation-deficient mutant named vagrant infection thread 1 (vag1) after suppressor mutant screening of spontaneous nodule formation 2, a cytokinin receptor gain-of-function mutant in Lotus japonicus. The VAG1 gene encodes a protein that is putatively orthologous to Arabidopsis ROOT HAIRLESS 1/HYPOCOTYL 7, a component of the plant DNA topoisomerase VI that is involved in the control of endoreduplication. Nodule phenotype of the vag1 mutant shows that VAG1 is required for the ploidy-dependent cell growth of rhizobial-infected cells. Furthermore, VAG1 mediates the onset of endoreduplication in cortical cells during early nodule development, which may be essential for the initiation of cortical cell proliferation that leads to nodule primordium formation. In addition, cortical infection is severely impaired in the vag1 mutants, whereas the epidermal infection threads formation is normal. This suggests that the VAG1-mediated endoreduplication of cortical cells may be required for the guidance of symbiotic bacteria to host meristematic cells.

The deubiquitinating enzyme AMSH1 is required for rhizobial infection and nodule organogenesis in Lotus japonicus

“…The infection mutants nap, pir, arpC1, cyclops and cerberus thus display abnormal IT development, but nodule organogenesis proceeds further than in amsh1. Conversely, loss of organogenesis-specific proteins, such as the cytokinin receptor LHK1 (Tirichine et al, 2006b(Tirichine et al, , 2007 and the DNA topoisomerase VI components VAG1 and SUNER1 (Suzaki et al, 2014;Yoon et al, 2014), does not hinder epidermal infection, but results in reduced or absent organogenesis. The nfr1, nfr5, symrk, nup133, nup85, castor, pollux, ccamk, pir and cyclops mutants all respond to cytokinin treatment with formation of nodule-like structures (Heckmann et al, 2011), making it unlikely that AMSH1 targeting of one of the corresponding proteins explains the requirement for AMSH1 downstream of cytokinin signaling.…”

Building the interaction interfaces: host responses upon infection with microorganisms

“…Similarly, RNS requires endoreduplication for nodule development. A mutation in VAG1 (vagrant infection thread1) in L. japonicus impairs nodule organogenesis due to the impairment of endoreduplication, though epidermal events such as IT formation are not affected in the mutant [64 ]. SUNERGOS1 in L. japonicus is involved in the ploidy of nodule cells and affects nodule organogenesis [65 ].…”

Comparison of the genome size, endoreduplication, and ISSR marker polymorphism in eight Lotus (Fabaceae) species

“…This phenomenon is a consequence of endoreduplication, a process during which nuclei undergo repeated rounds of DNA replication without mitosis. Knowledge of endopolyploidy in the genus Lotus is very scarce; it has been detected in roots of L. corniculatus and L. uliginosus, and in root nodules of L. japonicus, but not in leaves, petioles, stems, and petals of these species (Blair et al, 1988;González-Sama et al, 2006;Bainard et al, 2012;Suzaki et al, 2014). Endoreduplication is a genetically determined process and is species-specific (Sliwinska and Lukaszewska, 2005;Lukaszewska and Sliwinska, 2007;Sliwinska et al, 2012;Sliwinska, 2012, 2014).…”