8.8
TFs-miRNA: Regulating Copper Homeostasis
In plants, the micronutrient, copper (Cu) plays indispensable role in plant growth and
development by serving as an essential cofactor for many proteins operative in
biological processes like photosynthesis, ethylene perception, ROS detoxification,
and cell wall metabolism (Marschner 1995; Burkhead et al. 2009). The protein
classes that require Cu as a cofactor mainly belong to plastocyanin, copper/zinc
(Cu/Zn) superoxide dismutase (CSD), cytochrome c oxidase, plantacyanin
(plastocyanin-like copper containing proteins), ethylene receptors, salicylic acid
receptor NPR1, ascorbate oxidases, amine oxidases, polyphenol oxidase, and
laccases (Carr and Winge 2003; Weigel et al. 2003; Kuper et al. 2004; Mayer
2006; Puig et al. 2007; Burkhead et al. 2009; Wu et al. 2012). Deep investigation
on copper homeostasis in diverse plant species has delineated the conserved regulatory TF:Cu-miRNAs:target modules. Under limited Cu availability, plants activate
the Cu-economy mode wherein the activation of Cu-sensing transcription results in
the transcriptional activation of several Cu-miRNAs (Yamasaki et al. 2007). This
leads to the mRNA cleavage of the non-essential copper requiring proteins to save
copper for the most crucial and abundant protein plastocyanin and cytochrome
oxidase, which is required for plant autotrophic growth. Among the known
Cu-miRNAs miR408, miR398, and miR397 are conserved in plants, while few
miRNAs are species-specific including miR528 (monocot specific), miR508 (grapevine), miR1444 (popular), miR1073 (mosses), and miR857 (Arabidopsis) (Sunkar
et al. 2006; Yamasaki et al. 2007; Abdel-Ghany and Pilon 2008; Zhang and Li 2013;
Balyan et al. 2017). The transcriptional regulation of the above Cu-miRNAs in
response to Cu requires the conserved TF AtSPL7 in Arabidopsis (Yamasaki et al.
2009) and OsSPL9 (Balyan et al. 2017) in rice. The above SPL members share
similarity with Chlamydomonas reinhardtii CRR1 (copper response regulator),
which is the transcriptional regulator of Cu-homeostasis (Kropat et al. 2005).
AtSPL7, CRR1, and OsSPL9 bind to the Cu-response element (CuRE) having
GTAC core cis-regulatory motif in the promoter regions of their target MIR genes
and other protein genes like copper transporters (COPTs) (Kropat et al. 2005;
Yamasaki et al. 2009; Balyan et al. 2017). In Arabidopsis, SPL7 regulates the
transcription of MIR398, MIR408, MIR857, MIR397, MIR159, COPT1, COPT2,
ZIP2, FRO3, COPT6, and CCH, as well as a large number of genes involved in the
photosynthesis process (Yamasaki et al. 2009; Jung et al. 2012; Zhang et al. 2014a).
While in rice, OsSPL9 regulates miR408 and miR528 expression (Balyan et al.
2017; Yao et al. 2019; Yang et al. 2019). In addition, elongated Hypocotyl 5 (HY5, a
bzip TF), the master regulator of light signaling regulates the transcription of
MIR408 in Arabidopsis (Zhang et al. 2011, 2014a). The transcription of MIR408 is
co-regulated by SPL7 and HY5 in Arabidopsis under changing light and copper
regimens (Zhang et al. 2011, 2014a; Zhang and Li 2013). The target prediction,
experimental evidences, and degradome sequencing provide evidence that the
majority of the target genes of the above described Cu-miRNA encode for proteins
that require 1–4 Cu molecules as cofactors. The very first Cu-responsive miRNA,
miR398 targets the CSD1, CSD2, CCS1, blue copper-binding protein (BCBP) and a
8 Orchestration of MicroRNAs and Transcription Factors in the Regulation of Plant. . .
265
TFs-miRNA: Regulating Copper Homeostasis
In plants, the micronutrient, copper (Cu) plays indispensable role in plant growth and
development by serving as an essential cofactor for many proteins operative in
biological processes like photosynthesis, ethylene perception, ROS detoxification,
and cell wall metabolism (Marschner 1995; Burkhead et al. 2009). The protein
classes that require Cu as a cofactor mainly belong to plastocyanin, copper/zinc
(Cu/Zn) superoxide dismutase (CSD), cytochrome c oxidase, plantacyanin
(plastocyanin-like copper containing proteins), ethylene receptors, salicylic acid
receptor NPR1, ascorbate oxidases, amine oxidases, polyphenol oxidase, and
laccases (Carr and Winge 2003; Weigel et al. 2003; Kuper et al. 2004; Mayer
2006; Puig et al. 2007; Burkhead et al. 2009; Wu et al. 2012). Deep investigation
on copper homeostasis in diverse plant species has delineated the conserved regulatory TF:Cu-miRNAs:target modules. Under limited Cu availability, plants activate
the Cu-economy mode wherein the activation of Cu-sensing transcription results in
the transcriptional activation of several Cu-miRNAs (Yamasaki et al. 2007). This
leads to the mRNA cleavage of the non-essential copper requiring proteins to save
copper for the most crucial and abundant protein plastocyanin and cytochrome
oxidase, which is required for plant autotrophic growth. Among the known
Cu-miRNAs miR408, miR398, and miR397 are conserved in plants, while few
miRNAs are species-specific including miR528 (monocot specific), miR508 (grapevine), miR1444 (popular), miR1073 (mosses), and miR857 (Arabidopsis) (Sunkar
et al. 2006; Yamasaki et al. 2007; Abdel-Ghany and Pilon 2008; Zhang and Li 2013;
Balyan et al. 2017). The transcriptional regulation of the above Cu-miRNAs in
response to Cu requires the conserved TF AtSPL7 in Arabidopsis (Yamasaki et al.
2009) and OsSPL9 (Balyan et al. 2017) in rice. The above SPL members share
similarity with Chlamydomonas reinhardtii CRR1 (copper response regulator),
which is the transcriptional regulator of Cu-homeostasis (Kropat et al. 2005).
AtSPL7, CRR1, and OsSPL9 bind to the Cu-response element (CuRE) having
GTAC core cis-regulatory motif in the promoter regions of their target MIR genes
and other protein genes like copper transporters (COPTs) (Kropat et al. 2005;
Yamasaki et al. 2009; Balyan et al. 2017). In Arabidopsis, SPL7 regulates the
transcription of MIR398, MIR408, MIR857, MIR397, MIR159, COPT1, COPT2,
ZIP2, FRO3, COPT6, and CCH, as well as a large number of genes involved in the
photosynthesis process (Yamasaki et al. 2009; Jung et al. 2012; Zhang et al. 2014a).
While in rice, OsSPL9 regulates miR408 and miR528 expression (Balyan et al.
2017; Yao et al. 2019; Yang et al. 2019). In addition, elongated Hypocotyl 5 (HY5, a
bzip TF), the master regulator of light signaling regulates the transcription of
MIR408 in Arabidopsis (Zhang et al. 2011, 2014a). The transcription of MIR408 is
co-regulated by SPL7 and HY5 in Arabidopsis under changing light and copper
regimens (Zhang et al. 2011, 2014a; Zhang and Li 2013). The target prediction,
experimental evidences, and degradome sequencing provide evidence that the
majority of the target genes of the above described Cu-miRNA encode for proteins
that require 1–4 Cu molecules as cofactors. The very first Cu-responsive miRNA,
miR398 targets the CSD1, CSD2, CCS1, blue copper-binding protein (BCBP) and a
8 Orchestration of MicroRNAs and Transcription Factors in the Regulation of Plant. . .
265