@article{d715cb88974149488c6d9f33d5924527,
title = "Plant glutamate receptors mediate a bet-hedging strategy between regeneration and defense",
abstract = "Wounding is a trigger for both regeneration and defense in plants, but it is not clear whether the two responses are linked by common activation or regulated as trade-offs. Although plant glutamate-receptor-like proteins (GLRs) are known to mediate defense responses, here, we implicate GLRs in regeneration through dynamic changes in chromatin and transcription in reprogramming cells near wound sites. We show that genetic and pharmacological inhibition of GLR activity increases regeneration efficiency in multiple organ repair systems in Arabidopsis and maize. We show that the GLRs work through salicylic acid (SA) signaling in their effects on regeneration, and mutants in the SA receptor NPR1 are hyper-regenerative and partially resistant to GLR perturbation. These findings reveal a conserved mechanism that regulates a trade-off between defense and regeneration, and they also offer a strategy to improve regeneration in agriculture and conservation.",
keywords = "callus formation, developmental genetics, ion channel signaling, plant biotechnology, plant defense, plant regeneration, root development, salicyclic acid signaling, stem cells",
author = "Marcela Hern{\'a}ndez-Coronado and {Dias Araujo}, {Poliana Coqueiro} and Ip, {Pui Leng} and Nunes, {Cust{\'o}dio O.} and Ramin Rahni and Wudick, {Michael M.} and Lizzio, {Michael A.} and Feij{\'o}, {Jos{\'e} A.} and Birnbaum, {Kenneth D.}",
note = "Funding Information: To test the role of SA in GLR-mediated regeneration response, we assayed several mutants of the SA signal transduction pathway for regeneration phenotypes, with the receptor, NPR1, showing the most dramatic effect (Ding et al., 2018; Figures S5A–S5D). Compared with wild type, callus formation in the npr1-5 mutant showed more than a 3-fold increase, including more complete reprogramming of explants to callus (Figures 5A and 5B). In root-from-leaf regeneration, the npr1 mutant showed more than a 2-fold increase in efficiency (Figures 5C and 5D) and, similarly, in the root-from-stump assay, npr1 roots showed an approximate 2-fold increase in regeneration in high cuts (Figure 5E). Consistently, transient treatment with the SA inhibitor 4-phenyl-2-{[3-(trifluoromethyl)-aniline]methylidene}cyclohexane-1,3-dione (PAMD) showed higher regeneration than mock-treated wild-type roots in all three regeneration systems, although PAMD has a strong inhibitory effect on long-term growth (Figures 5A–5E; Seo et al., 2012). In contrast, treatment of roots with SA greatly inhibited regeneration in all the systems tested (Figures 5A–5D, S5E, and S5F). These strong effects with transient treatments support a role for SA signaling in the inhibition of regeneration in the post-injury environment.Examining epistatic effects between the GLR and SA pathway, we observed at least partial insensitivity of npr1 to regeneration enhancement by CNQX treatment in most assays (Figures 5A–5D). The insensitivity of npr1 to CNQX was most apparent in the more challenging regeneration assays, such as high cuts in root-from-stump regeneration (Figures S5A and S5D). In addition, although wild-type plants showed increased regeneration in SA inhibitor PAMD, the same treatment had no effect on regeneration in the glr1.2/1.4/2.2/3.3 mutant combination, showing resistance to the SA inhibitor (Figure S5E). The results are consistent with GLR perturbations already suppressing downstream SA signaling. Simultaneous treatment with CNQX and SA in wild-type plants showed only a small, non-significant decrease in root regeneration levels compared with CNQX treatment alone (Figure 5F). However, treatment of the glr1.2/1.4/2.2/3.3 mutant with SA still inhibits regeneration as it does in wild type, a partial rescue of the wild-type response by apparent restoration of downstream SA signaling (Figure S4E). These results support a role for SA downstream of GLR signaling. Together, the results suggest that the GLR-mediated effects on regeneration work in large part through the SA signaling pathway.We thank Carlos Ortiz-Ram{\'i}rez for helpful input on GLRs. K.D.B. is supported by the National Institutes of Health (R35GM136362) and the National Science Foundation (1934388). J.A.F. was supported by the NIH (R01-GM131043) and the NSF (MCB-1930165). Conceptualization, M.H.C, P.C.D.A. and K.D.B.; methodology, M.H.C, P.C.D.A. C.O.N, J.A.F. and K.D.B.; materials and expertise, M.M.W. and M.A.L.; experiments, M.H.C. P.C.D.A. P.-L.I, C.O.N. R.R. and M.A.L.; data analysis, M.H.C. P.C.D.A. C.O.N. J.A.F. and K.D.B.; writing, M.H.C. and K.D.B. A patent (application #63120640) has been filed related to this work on compositions and methods to enhance plant regeneration. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in science. One or more of the authors of this paper self-identifies as a member of the LGBTQ+ community. The author list of this paper includes contributors from the location where the research was conducted who participated in the data collection, design, analysis, and/or interpretation of the work. While citing references scientifically relevant for this work, we also actively worked to promote gender balance in our reference list. Funding Information: We thank Carlos Ortiz-Ram{\'i}rez for helpful input on GLRs. K.D.B. is supported by the National Institutes of Health (R35GM136362) and the National Science Foundation (1934388). J.A.F. was supported by the NIH (R01-GM131043) and the NSF (MCB-1930165). Publisher Copyright: {\textcopyright} 2022 Elsevier Inc.",
year = "2022",
month = feb,
day = "28",
doi = "10.1016/j.devcel.2022.01.013",
language = "English (US)",
volume = "57",
pages = "451--465.e6",
journal = "Developmental Cell",
issn = "1534-5807",
publisher = "Cell Press",
number = "4",
}