The PIF1-miR408-PLANTACYANIN repression cascade regulates light-dependent seed germination

Abstract

Light-dependent seed germination is a vital process for many seed plants. A decisive event in light-induced germination is degradation of the central repressor PHYTOCHROME INTERACTING FACTOR 1 (PIF1). The balance between gibberellic acid (GA) and abscisic acid (ABA) helps to control germination. However, the cellular mechanisms linking PIF1 turnover to hormonal balancing remain elusive. Here, employing far-red light-induced Arabidopsis thaliana seed germination as the experimental system, we identified PLANTACYANIN (PCY) as an inhibitor of germination. It is a blue copper protein associated with the vacuole that is both highly expressed in mature seeds and rapidly silenced during germination. Molecular analyses showed that PIF1 binds to the miR408 promoter and represses miR408 accumulation. This in turn posttranscriptionally modulates PCY abundance, forming the PIF1-miR408-PCY repression cascade for translating PIF1 turnover to PCY turnover during early germination. Genetic analysis, RNA-sequencing, and hormone quantification revealed that PCY is necessary and sufficient to maintain the PIF1-mediated seed transcriptome and the low-GA-high-ABA state. Furthermore, we found that PCY domain organization and regulation by miR408 are conserved features in seed plants. These results revealed a cellular mechanism whereby PIF1-relayed external light signals are converted through PCY turnover to internal hormonal profiles for controlling seed germination.

The Copper Responsive Transcription Factor SPL7 Represses Key Abscisic Acid Biosynthetic Genes to Balance Growth and Drought Tolerance

“…Second, we showed in the current study that functional GTAC Cu-response motifs are present in the promoters of key ABA biosynthetic genes in phylogenetically representative land plant species (Figure 12 and 13; Supplemental Figure 9 to 11). Additionally, the phenomenon that high Cu increases ABA accumulation has been reported by physiological studies in different plant species (An et al, 2008; Ye et al, 2014; Jiang et al, 2021). Repression of ABA biosynthesis by the SPL7-GTAC circuit thus appears to be a conserved mechanism in land plants.…”

“…ABA level in spl7-ko was not further increased by high Cu exposure (Figure 10A). Moreover, we measured ABA content in the wild type and spl7-ko plants at checkpoint III using both the ELISA method and the ultrahigh-performance liquid chromatography-triple quadrupole mass spectrometry (UPLC-MS/MS) method (Fu et al, 2012; Jiang et al, 2021). These analyses confirmed that the amount of ABA was significantly higher in spl7-ko than in the wild type plants (Figure 10B and 10C).…”

“…These results support a scenario in which SPL7 regulates Cu partitioning based on the prevailing Cu condition to balance growth and drought tolerance (Figure 14). Under low Cu, in addition to activating the Cu-microRNAs that favor Cu allocation to the plastocyanin for photosynthesis (Yamasaki et al, 2009; Zhang et al, 2014; Pan et al, 2018; Jiang et al, 2021), direct repression of key ABA biosynthetic genes by SPL7 results in diminished ABA production to promote growth (Figure 4 and 10 to 12). Under high Cu, degradation of SPL7 releases suppression on ABA biosynthesis and high ABA in turn enhances stress tolerance.…”

“…In higher plants, Cu is required for growth because the small blue Cu protein plastocyanin, abundantly present in the thylakoid lumen, is an indispensable electron carrier in the Z-scheme of photosynthesis (Molina-Heredia et al, 2003; Weigel et al, 2003). Given that Cu is involved in the synthesis or perception of stress related hormones including ABA (Peñarrubia et al, 2015; Jiang et al, 2021) and ethylene (Rodríguez et al, 1999), is required for the making of protective structures such as lignin (Zhao et al, 2013; Reyt et al, 2020; Zhuang et al, 2020), and participates in various stress responses (Pätsikkä et al, 2002; Abdel-Ghany, 2009; Yamasaki et al, 2009), a role for Cu homeostasis in balancing growth and stress responses warrants investigation.…”

OPT3 Transports Copper to the Phloem, Mediates Shoot-to-Root Copper Signaling and Crosstalk Between Copper and Iron Homeostasis inA. thaliana

“…In addition to these processes, copper is involved in cell wall lignification and reproduction (Epstein and Bloom, 2005;Broadley et al, 2012;Chen et al, 2020;. Recent studies implicate copper in light-dependent seed germination (Jiang et al, 2020), shaping the shoot architecture, transition to flowering, stigmatic papillae development and senescence (Rahmati . Mounting evidence from studies in animal species also implicates copper in cell signaling through its untraditional role as a modulator of MAPK signaling and mTORdependent autophagic kinase signaling (Turski and Thiele, 2009;Turski et al, 2012;Chang, 2015;Tsang et al, 2020).…”