ALTERED MERISTEM PROGRAM1 Restricts Shoot Meristem Proliferation and Regeneration by Limiting HD-ZIP III-Mediated Expression of RAP2.6L

Abstract

Plants show an indeterminate mode of growth by the activity of organ forming stem cell niches in apically positioned meristems. The correct formation and activity of these meristems are a prerequisite for their adaptive development and also allow the maintenance of organogenesis under adverse circumstances such as wounding. Mutation of the putative Arabidopsis () Glu carboxypeptidase ALTERED MERISTEM PROGRAM1 (AMP1) results in Arabidopsis plants with enlarged shoot apical meristems, supernumerary stem cell pools, and higher leaf formation rate. AMP1 deficiency also causes exaggerated de novo formation of shoot meristems. The activity of AMP1 has been implicated in the control of microRNA (miRNA)-dependent translation; however, it is not known how this function contributes to the shoot meristem defects. Here, we show that the transcription factor RAP2.6L is upregulated in the Arabidopsis mutant. Overexpression of RAP2.6L in the wild type causes mutant-related phenotypic and molecular defects, including enhanced shoot regeneration in tissue culture. Conversely, inhibition of RAP2.6L in the mutant suppresses stem cell hypertrophy and the regenerative capacity. We further provide evidence that is under direct transcriptional control of miRNA-regulated class III homeodomain-Leu zipper (HD-ZIP III) proteins, key regulators of shoot meristem development, which overaccumulate in the mutant. Our results reveal a transcription factor module acting downstream of in the control of shoot stem cell niche patterning. By positioning the HD-ZIP III/RAP2.6L module downstream of AMP1 function, we provide a mechanistic link between the role of AMP1 in miRNA-mediated translational repression and shoot stem cell specification.

AMP1 and CYP78A5/7 act through a common pathway to govern cell fate maintenance in Arabidopsis thaliana

“…The latter is supported by a recent study, in which no translational de-repression of miR156 target SPL9 or the miR159 target MYB33 could be observed in amp1 [41]. We showed that AMP1 acts through the AP2 transcription factor RAP2.6L, which is controlled by the miRNA-regulated HD-ZIP III proteins [22] and we are currently analyzing the functional relationship between HD-ZIP III mis-regulation and amp1 phenotypes. Notably, RAP2.6L expression is up-regulated in cyp78a5,7 and coincides with enhanced protein levels of the HD-ZIP III member PHV.…”

“…This discrepancy might be caused by a locally restricted release of translational repression in the AMP1/LAMP1 expression domain affecting only a subset of miRNA targets. Recently, indirect evidence was provided that the over-accumulation of the miRNA-controlled HD-ZIP III proteins contributes to the shoot phenotype of amp1 [22]. However, several other miRNA-targets have been shown to be mis-regulated in the mutant and their phenotypic impact has yet to be revealed.…”

ETHYLENE RESPONSE FACTOR 115 integrates jasmonate and cytokinin signaling machineries to repress adventitious rooting in Arabidopsis

“…Recently, Zhou and collaborators (Zhou et al ., 2019) showed that two members of subgroup X of the APETALA2/ETHYLENE RESPONSE FACTOR (ERF) family ( ERF109 and ERF115 ) promote root stem cell niche replenishment and tissue regeneration after excision, and their expression is directly controlled by MYC2‐mediated JA signaling. The ERF115 transcription factor and its two closest homologs, ERF114 (also known as ERF BUD ENHANCER ( EBE )) and ERF113 (also known as RELATED to AP2.6L , RAP2.6L ) have been shown to control various regenerative processes, such as callus formation, tissue repair, root stem cell niche maintenance and root growth (Che et al ., 2006; Nakano et al ., 2006; Asahina et al ., 2011; Mehrnia et al ., 2013; Heyman et al ., 2016; Ikeuchi et al ., 2018; Kong et al ., 2018; Yang et al ., 2018). The three genes are rapidly induced by mechanical wounding (Ikeuchi et al ., 2017), suggesting that they play an important role in connecting the stress‐induced JA signaling machinery with other signaling cascades in provision of correct cell‐fate and/or developmental inputs for organogenesis processes.…”

ALTERED MERISTEM PROGRAM1regulates leaf identity independent of miR156-mediated translational repression

“…amp1-1 (hereafter, amp1 ) mutants resemble plants with reduced SPL gene expression in having an increased rate of leaf initiation, an increased number of rosette leaves, an enlarged shoot apical meristem, and small, round rosette leaves that lack abaxial trichomes (Fig. 1A-F) (Chaudhury et al, 1993; Huang et al, 2015; Telfer et al, 1997; Yang et al, 2018). To determine if this phenotype is attributable to a reduction in SPL activity, we introduced 35S::MIM156 — which de-represses SPL gene expression (Franco-Zorrilla et al, 2007) — into amp1 .…”