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Shigenaga, A. M.

Publications and source records attributed to Shigenaga, A. M..

3 recordsLinked to original sources

The Sulfated PSY Peptide Negatively Regulates Receptor Kinase Activity to Promote Growth

Complex signaling pathways organize cell expansion and proliferation across cells to pattern tissues and organs in plants. The sulfotyrosine peptide hormone family, PLANT PEPTIDE CONTAINING SULFATED TYROSINE (PSY), contributes to these processes. We identified two plasma membrane-localized receptors, PSYR1 and PSYR2, that are necessary for PSY signaling and regulate growth in Physcomitrium patens. Membrane-associated PSYRs accumulate to high levels in a mutant lacking TYROSYL PROTEIN SULFOTRANSFERASE (TPST). Given that a tpst null mutant ({triangleup}tpst) is impaired in sulfation, this suggests that in the absence of sulfated peptides, PSYRs accumulate on the membrane. A null mutant of the PSY receptors,{triangleup} psyr1/2, showed increased growth and was epistatic to{triangleup} tpst, suppressing defects in gametophore formation and early senescence. The transcriptional profiles comparing wild type to{triangleup} psyr1/2 and{triangleup} psyr1/2/{triangleup}tpst showed 25 to 30 differentially expressed genes between the receptor null mutants and wild type, with a common signature of cell wall remodeling and stress responses. Similarly, a PSYR1 kinase-inactive mutation rescued{triangleup} tpst and relieved the accumulation of membrane-associated PSYRs. In contrast, overexpression of PSYRs inhibited plant growth, with phenotypic severity correlating with the amount of overexpression. These data are consistent with a constitutive activation model in which membrane-associated PSYRs unbound to PSY serve to inhibit growth through an active kinase. In the presence of the PSY peptide, the kinase is inactivated, promoting growth and driving PSY expression. The relationship between growth-repressive PSYR kinase activity and growth-promoting PSYR kinase inactivation in P. patens serves as a model for optimizing plant growth and development.

plant biology↗

Evidence for Early Evolution of Sulfated Peptide Signaling in Plant Development

In plants, the cell wall fixes the position of each cell; therefore, during development, plants rely on cellular proliferation and expansion for tissue patterning and organ formation. How plant cells communicate with neighboring cells to coordinate expansion for properly patterned tissues and organs is not well understood. In seed plants, organ growth is known to be modulated by sulfotyrosyl peptide signaling. Here, we report that the activity of TYROSYL PROTEIN SULFOTRANSFERASE (TPST), which is responsible for the post-translational modification of sulfotyrosyl peptides, is essential for expansion during development in the non-vascular plant, Physcomitrium patens. Plants that harbor a null mutation in the gene encoding TPST ({Delta}tpst) were smaller, formed fewer caulonemal filaments, and were unable to form expanded gametophores. In {Delta}tpst multiple aspects of gametophore development were affected, including the first division of the gametophore initial, as well as reduced rates of cell division and expansion. Mutational analysis of P. patens TPST identified the residue Histidine 124, a candidate catalytic residue, as essential for TPST function. Notably, addition of the sulfated signaling peptide, PSY1 from either P. patens or Arabidopsis thaliana, rescued all {Delta}tpst developmental deficits. Taken together, these data suggest that TPST functions to sulfate PSY, and this activity is necessary for plant growth and development. Furthermore, since addition of AtPSY fully rescues {Delta}tpst and PpPSY promotes root elongation in Arabidopsis and rice, these findings suggest that PSY signaling is evolutionarily conserved.

developmental biology↗

Reduced methane emissions in transgenic rice genotypes are associated with altered rhizosphere microbial hydrogen cycling

Rice paddies contribute substantially to atmospheric methane (CH4) and these emissions are expected to increase as the need to feed the human population grows. Here, we show that two independent rice genotypes overexpressing genes for PLANT PEPTIDES CONTAINING SULFATED TYROSINE (PSY) reduced cumulative CH4 emissions by 38% (PSY1) and 58% (PSY2) over the growth period compared with controls. Genome-resolved metatranscriptomic data from rhizosphere soils reveal lower ratios of gene activities for CH4 production versus consumption, decrease in activity of H2-producing genes, and increase in bacterial H2 oxidation pathways in the PSY genotypes. Metabolic modeling using metagenomic and metabolomic data predicts elevated levels of H2 oxidation and suppressed H2 production in the PSY rhizosphere. The H2-oxidizing bacteria have more genes for utilization of gluconeogenic acids than H2-producing counterparts, and their activities were likely stimulated by the observed enrichment of gluconeogenic acids (mostly amino acids) in PSY root exudates. Together these results suggest that decreased CH4 emission is due to the reduction of H2 available for hydrogenotrophic methanogenesis. The combination of rice phenotypic characterization, microbiome multi-omic analysis, and metabolic modeling described here provides a powerful strategy to discover the mechanisms by which specific plant genotypes can alter biogeochemical cycles to reduce CH4 emissions.

microbiology↗