Legumes, unlike most land plants, can form a root nodule symbiosis with nitrogen-fixing rhizobia. The anatomy of the nodule in legume plants was described in the 17^th century, and nodule cells were found to host endosymbiotic rhizobia for nitrogen fixation in the 19^th century. The legume cortex is developmentally distinct from the cortex of non-legumes: it can de-differentiate in response to phytohormones or symbiotic signals from rhizobia, thereby enabling de novo organogenesis of nodules to accommodate nitrogen-fixing rhizobia. Nevertheless, why symbiotic nitrogen fixation is restricted to relatively few plant species, mainly in legumes, has remained unknown.

Recently, a research group led by Prof. Wang Ertao from CAS Center for Excellence in Molecular Plant Sciences, found that the ancient SHORTROOT-SCARECROW (SHR-SCR) stem cell program in cortical cells of the legume Medicago truncatula specifies their distinct fate for novel nodule organogenesis.

In this study, to identify potential genetic pathway reprogramming events that underlie the cortical cell division response in legumes, the researchers generated EGFP-β-Glucuronidase reporters (promoter:EGFP-GUS) for M. truncatula and A. thaliana genes and found that the MtSCR reporter was highly expressed in M. truncatula endodermis, cortex and epidermis, which is in sharp contrast to A. thaliana AtSCR. Further genetic data show that nodule formations in scr and scr/scl23 mutants were greatly reduced and SCR expression in root cortex is required for cortical cell division during nodule initiation.

The researchers found that MtSHR1/2 mRNA expression is restricted to the stele, similar to the expression pattern of AtSHR in A. thaliana. Intriguingly, MtSHR-GUS fusion proteins accumulated GUS staining beyond the stele and endodermis, in the epidermis and cortex. Genetic data show that cortical cell-specific accumulation of MtSHRs is required for cortical cell division during nodule initiation. Rhizobia spot inoculation and cytokinin treatment showed that cortical cell expressed MtSHR-MtSCR controls M. truncatula root cortical cells division ability.

Further studies revealed that rhizobial signals lead to the accumulation of MtSHR-MtSCR in cortical cells and nodule primordia. Ubiquitously overexpressed MtSHR in M. truncatula hairy roots promote cortical cell division and form pseudo-nodules without rhizobia inoculation. These data together demonstrate that the ancient SHR-SCR stem cell program specifies legume cortical cell fate for novel nodule organogenesis.

This work was published online in Nature entitled "An SHR–SCR module specifies legume cortical cell fate to enable nodulation " on December 10^th.

This work was supported by the Strategic Priority Research Program ‘Molecular Mechanism of Plant Growth and Development’ of the Chinese Academy of Sciences, the National Science Foundation, and the Youth Innovation Promotion Association.

Cortical cell division competence for nodule organogenesis in legumes.

a, The MtSHR-MtSCR network in cortical cells allows them to respond to symbiotic signals and cytokinins. b, Rhizobial signals activate the MtSHR/MtSCR module to promote cortical cell division and nodule organogenesis.

Link: https://www.nature.com/articles/s41586-020-3016-z

Contact:
Dr. Ertao Wang, Professor
National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences (CEMPS), Chinese Academic of Sciences
Tel: 86-21-54924081
Email: etwang@cemps.ac.cn