A Jasmonate Signaling Network Activates Root Stem Cells and Promotes Regeneration

Abstract

Plants are sessile and have to cope with environmentally induced damage through modification of growth and defense pathways. It is an open question how tissue regeneration is triggered in such responses and whether this involves stem cell activation. The stress hormone jasmonate (JA) plays well-established roles in wounding and defense responses. JA also affects growth which is hitherto interpreted as trade-off between growth and defense. Here, we describe a molecular network triggered by wound-induced JA that promotes stem cell activation and regeneration. JA regulates organizer cell activity in the root stem cell niche through the RBR-SCR network and stress response protein ERF115. Moreover, JA-induced ERF109 transcription stimulates CYCD6;1 expression, functions upstream of ERF115 and promotes regeneration. Soil penetration and response to nematode herbivory induce and require this JA mediated regeneration response. Therefore, the JA tissue damage response pathway induces stem cell activation and regeneration, and activates growth after environmental stress. Results JA acts through RBR-SCR to regulate quiescenceWe confirmed that JA promotes division of QC cells (Chen et al., 2011) ( Figures 1A and 1B, S1B and S1C), and that extra QC divisions occur in plants with altered SCR-RBR network:pWOX5::amiGORBR, which specifically downregulates RBR in the QC, and pSCR::SCRaca-YFP, which specifically disrupts RBR-SCR protein interaction (Cruz-Ramirez et al., 2013) ( Figures 1D and 1G). We observed QC divisions in wild type Col-0 after 50 µM or 100 µM MeJA (methyl ester of JA) treatment for 48 hours ( Figures 1A-1C and 1J), respectively. Conversely, no extra QC divisions were detected in pWOX5::amiGORBR and pSCR::SCRaca-YFP lines treated with 50 µM or 100 µM MeJA for the same period (Figures 1D-1I and 1K-1L), suggesting that JA may function through the SCR-RBR network in regulating quiescence of QC. To further confirm this, we introgressed the JA receptor loss of function mutant allele coi1-2 (Xu et al., 2002) into pWOX5::amiGORBR and pSCR::SCRaca-YFP lines. The QC division phenotypes and QC cell numbers of these introgression lines revealed no differences to pSCR::SCRaca-YFP and pWOX5::amiGORBR lines, both with and without MeJA treatment, respectively ( Figures S1D-S1M). These findings position SCR and RBR downstream of COI1 to control quiescence of QC. After MeJA treatment, QC cell numbers of scr-3 and shr-2 mutants did not increase significantly compared to controls ( Figures S1N-S1T), confirming that JA induces QC division through the SCR/SHR pathway. SCR and RBR expression levels were not altered significantly after MeJA treatment, judged by marker expression and reverse transcription-quantitative polymerase chain reaction (RT-qPCR) assays (Figures S1U-S1AA).These data indicate that JA does not regulate SCR and RBR at the gene expression level. JA directly induces ERF115 transcriptionThe AP2/ERF family transcription factor ERF115 was reported to control root QC cell division (Heyman et al., 2013). When 35S::ERF11...

Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

“…For example, Aphis gossypii spends a longer time feeding from the phloem in virus-infected plants than in non-infected plants, thus increasing the This sophisticated JA pathway can confer versatile and adaptive traits to plants by fine tuning the balance between defense and development [45]. Defective JA reception will aggravate the symptoms caused by RNA viruses, the nematode herbivory induces JA-mediated stem cell activation and regeneration, suggesting the critical roles of JA in plant developmental regulation [22,46]. Meanwhile, JAs and JA signaling serve multiple roles in response to herbivores by priming direct and indirect defenses of plants [47][48][49][50].…”

Identification of Shoot Differentiation-Related Genes in Populus euphratica Oliv.

“…The induced immune response functions to sterilize the site of injury and remove dead or dying cells, securing the maintenance of normal callus tissue, which constitutes a premise step for the cell fate conversion of stem cells. As a common role of jasmonate (JA) acting in pathophysiology and wound signaling [40], JA promotes stem cell activation and regeneration in stem cell niche through ERF115 [41]. In our study, two genes of ERF109 showed a −6.43 and −6.50 FC of down-regulation in the LD group.…”

AP2/ERF Transcription Factors Integrate Age and Wound Signals for Root Regeneration

“…It has been shown that JA activates root stem cells Marhava et al, 2019;Zhou et al, 2019). In addition, JA and ERF109 evoke auxin biosynthesis through ASA1 (Sun et al, 2009;Cai et al, 2014).…”

“…However, how these signals regulate gene expression in the nucleus is largely unknown. The identification of wound-induced AP2/ERFs suggests the early wound signal rapidly reprograms the transcriptome at the transcriptional level (Marhava et al, 2019;Zhang et al, 2019;Zhou et al, 2019). Intriguingly, studies from the Sugimoto lab have shown that another group of AP2/ERF-type transcriptional factor genes, named WOUND-INDUCED DEDIFFERENTIATION1 (WIND1) and its homologs WIND2, WIND3 and WIND4, is induced upon wounding (Iwase et al, 2011a;2011b).…”