The Plant Cell, Vol. 29: 1803–1805, August 2017, www.plantcell.org ã 2017 ASPB.
LETTER TO THE EDITOR
Reply: The BIF Domain Is Structurally and Functionally Distinct from Other Types of ACT-Like Domains OPEN
We welcome the discussion on the BIF/ACTlike domain in plant bHLH proteins and hope this will help to clarify their functions and structures distinct from those of other types of ACTlike proteins. The bHLH proteins are found in major eukaryotic groups and play important roles in many plant developmental processes and environmental responses (Feller et al., 2006; Pires and Dolan, 2010). The model plant Arabidopsis thaliana has 159 bHLH members; in particular, DYSFUNCTIONAL TAPETUM1 (DYT1) is an early regulator of normal tapetum and pollen development (Zhang et al., 2006; Feng et al., 2012; Zhu et al., 2015). DYT1 expression and function are precisely regulated by a set of interactions: On one hand, protein products of DYT1 downstream genes bHLH010/089/091 interact and form a feedforward loop with DYT1 to control the proper expression of shared downstream anther genes (Zhu et al., 2015); on the other hand, bHLH010/bHLH089/bHLH091 facilitates the stage-dependent nuclear-specific localization of DYT1 in a positive feedback regulatory loop enhancing DYT1 function (Cui et al., 2016). In addition to the bHLH domain, DYT1 and its homologs share a second domain close to its C terminus with a predicted secondary structure of bbabba (a for an a helix and b for a b strand) (Figure 1). This C-terminal domain of DYT1 is required for the interaction with and the nuclear localization by bHLH010/ bHLH089/bHLH091, and transcriptional activation activity and in vivo function of DYT1 (Cui et al., 2016); this domain in DYT1 and homologs was named the BIF domain for bHLH protein interaction and function and also found in over one-third of Arabidopsis bHLH proteins (Cui et al., 2016). Previously, a domain with similar predicted bbabba structure was found in the maize (Zea mays) bHLH transcription factor R and some additional maize and Arabidopsis proteins and was referred to as an ACT-like domain (Feller et al., 2006) or ACT domain (Kong et al., 2012). However, there are substantial functional and OPEN Articles can be viewed without a subscription. www.plantcell.org/cgi/doi/10.1105/tpc.17.00547
structural differences (see below) between the C-terminal BIF/ACT-like domain of plant bHLH proteins (Feller et al., 2006; Kong et al., 2012; Cui et al., 2016) and the original ACT domain and previously reported ACT-like domain in other proteins (Chipman and Shaanan, 2001; Siltberg-Liberles and Martinez, 2009; Lang et al., 2014). The ACT domain and previously reported ACT-like domains are found in functionally diverse proteins. The ACT domain, which was named after the three founding members aspartate kinase, chorismate mutase, and TyrA (prephenate dehydrogenase), is found in a variety of enzymes involved in amino acid and purine metabolism and is known to bind amino acids in negative feedback regulation of such enzymes (Schuller et al., 1995; Aravind and Koonin, 1999; Grant et al., 1999; Chipman and Shaanan, 2001; Grant et al., 2001). The ACT domain was thought to have evolved independently from the catalytic domain of amino acid metabolic enzymes (Hsieh and Goodman, 2002). The ACT domain is found in Arabidopsis amino acid metabolic enzymes such as aspartate kinase, 3-phosphoglycerate dehydrogenase, and acetohydroxyacid synthase regulatory subunit, with suggested regulatory functions (Chipman and Shaanan, 2001; Lee and Duggleby, 2001; Hsieh and Goodman, 2002; Mas-Droux et al., 2006). In addition, the ACT domain is present in ACT domain repeat (ACR) proteins in plants, with multiple members in both Arabidopsis and rice (Oryza sativa), including the OsACR7 and OsACR9, which likely act as the glutamine signal sensors (Hsieh and Goodman, 2002; Hayakawa et al., 2006; Liu, 2006; Kudo et al., 2008; Sung et al., 2011; Takabayashi et al., 2016)). The ACT and ACTlike domains in the regulatory domains of Escherichia coli threonine deaminase have similar babbab secondary structures (Schuller et al., 1995; Aravind and Koonin, 1999; Chipman and Shaanan, 2001; Lang et al., 2014). Another domain was considered to be an ACT-like domain because of a predicted babbab secondary structure similar to that of ACT-proteins, but it was named RAM, for regulation of amino acid metabolism (Ettema et al., 2002).
By contrast, the BIF/ACT-like domains in plant bHLH proteins are predicted to share a bbabba structure, which differs from the babbab structure in the position of four out ofsix motifs (Felleretal., 2006;Kongetal., 2012; Cui et al., 2016). At the sequence level, there are very low levels of amino acid sequence identities, with only 4.6% between the ACT domain of3-phosphoglyceratedehydrogenaseandthe ACT-like domain of threonine deaminase, and only 6.6% between the ACT domain and the ACT-like RAM domain; these percentages are not statistically different from that between two random sequences. The levels of amino acid sequence identities between the ACT-like domains in plant bHLH proteins and the ACT domains are also very low, such that the DYT1 and R proteins are not found in the Pfam database as having an ACT-like domain. In short, the “ACT-like domain” is a general termforvariousdomainsthatshowsimilarstructural similarities to the ACT domain, whereas the “BIF domain” is a more specific term referring to those in DYT1 and other plant bHLH proteins with distinct function in dimerization and nuclear localization of interacting proteins and the bbabba topology. We consider the domain in plant bHLH proteins sufficiently different from others to warrant a distinct name. Fang Chang,a Jie Cui,a Linbo Wang,a and Hong Maa ,b ,1 a State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering and Institute of Biodiversity Sciences, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200433, China b Center for Evolutionary Biology, Institutes of Biomedical Sciences, Fudan University, Shanghai 200433, China 1 Address
correspondence to hxm16@psu. edu.
ORCID ID: 0000-0001-8717-4422 (H.M.)
1804
The Plant Cell
Figure 1. The Location and Position (with P Value) of DYT1 Orthologs: Conserved Motifs in the DYT1 Sequence. (A) A schematic diagram representing the a-helices (magenta box) and b-sheets (green arrows) in DYT1. (B) A block diagram showing the eight best nonoverlapping tiling of motifs from the analysis of the DYT1 amino acid sequences and those of 54 DYT1 orthologs; the conserved motifs (M1;M8) are indicated as boxes with different colors. The length of each motif is relative to the length of DYT1 sequence, and the height of each box provides an indication of the significance of the match. (C) The location and amino acid sequences of each motif. Position P value (the probability of a single random subsequence of the length of the motif scoring at least as well as the observed match) is indicated above each motif. The secondary structure of DYT1 was predicted on the website https://www. predictprotein.org, and the motif analysis was performed using MEME software (Bailey and Elkan, 1994).
ACKNOWLEDGMENTS The BIF domain-related work was supported by grants from the Ministry of Science and Technology (2012CB910503) and the National Science Foundation of China (31130006 and 31070274). AUTHOR CONTRIBUTIONS F.C. and J.C. drafted an early version of the manuscript. F.C. prepared a new version of the manuscript with sequence analyses by L.W. H.M. discussed the manuscript with other authors and revised the manuscript. Received July 10, 2017; revised June 10, 2017; accepted July 26, 2017; published July 26, 2017.
REFERENCES Aravind, L., and Koonin, E.V. (1999). Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches. J. Mol. Biol. 287: 1023–1040. Bailey, T.L., and Elkan, C. (1994). Fitting a mixture model by expectation maximization
to discover motifs in biopolymers. University of California San Diego Technical Report CS94–351. Chipman, D.M., and Shaanan, B. (2001). The ACT domain family. Curr. Opin. Struct. Biol. 11: 694–700. Cui, J., You, C., Zhu, E., Huang, Q., Ma, H., and Chang, F. (2016). Feedback regulation of DYT1 by interactions with downstream bHLH factors promotes DYT1 nuclear localization and anther development. Plant Cell 28: 1078– 1093. Ettema, T.J.G., Brinkman, A.B., Tani, T.H., Rafferty, J.B., and Van Der Oost, J. (2002). A novel ligand-binding domain involved in regulation of amino acid metabolism in prokaryotes. J. Biol. Chem. 277: 37464–37468. Feller, A., Hernandez, J.M., and Grotewold, E. (2006). An ACT-like domain participates in the dimerization of several plant basic-helix-loophelix transcription factors. J. Biol. Chem. 281: 28964–28974. Feng, B., Lu, D., Ma, X., Peng, Y., Sun, Y., Ning, G., and Ma, H. (2012). Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J. 72: 612–624.
Grant, G.A., Hu, Z., and Xu, X.L. (2001). Specific interactions at the regulatory domain-substrate binding domain interface influence the cooperativity of inhibition and effector binding in Escherichia coli D-3-phosphoglycerate dehydrogenase. J. Biol. Chem. 276: 1078– 1083. Grant, G.A., Kim, S.J., Xu, X.L., and Hu, Z. (1999). The contribution of adjacent subunits to the active sites of D-3-phosphoglycerate dehydrogenase. J. Biol. Chem. 274: 5357–5361. Hayakawa, T., Kudo, T., Ito, T., Takahashi, N., and Yamaya, T. (2006). ACT domain repeat protein 7, ACR7, interacts with a chaperone HSP18.0-CII in rice nuclei. Plant Cell Physiol. 47: 891–904. Hsieh, M.H., and Goodman, H.M. (2002). Molecular characterization of a novel gene family encoding ACT domain repeat proteins in Arabidopsis. Plant Physiol. 130: 1797–1806. Kong, Q., Pattanaik, S., Feller, A., Werkman, J.R., Chai, C., Wang, Y., Grotewold, E., and Yuan, L. (2012). Regulatory switch enforced by basic helix-loop-helix and ACT-domain mediated dimerizations of the maize transcription factor R. Proc. Natl. Acad. Sci. USA 109: E2091–E2097.
August 2017
Kudo, T., Kawai, A., Yamaya, T., and Hayakawa, T. (2008). Cellular distribution of ACT domain repeat protein 9, a nuclear localizing protein, in rice (Oryza sativa). Physiol. Plant. 133: 167–179. Lang, E.J., Cross, P.J., Mittelsta¨dt, G., Jameson, G.B., and Parker, E.J. (2014). Allosteric ACTion: the varied ACT domains regulating enzymes of amino-acid metabolism. Curr. Opin. Struct. Biol. 29: 102–111. Lee, Y.T., and Duggleby, R.G. (2001). Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry 40: 6836–6844. Liu, Q. (2006). Computational identification and systematic analysis of the ACR gene family in Oryza sativa. J. Plant Physiol. 163: 445–451. Mas-Droux, C., Curien, G., Robert-Genthon, M., Laurencin, M., Ferrer, J.L., and Dumas,
R. (2006). A novel organization of ACT domains in allosteric enzymes revealed by the crystal structure of Arabidopsis aspartate kinase. Plant Cell 18: 1681–1692. Pires, N., and Dolan, L. (2010). Origin and diversification of basic-helix-loop-helix proteins in plants. Mol. Biol. Evol. 27: 862–874. Schuller, D.J., Grant, G.A., and Banaszak, L.J. (1995). The allosteric ligand site in the Vmax-type cooperative enzyme phosphoglycerate dehydrogenase. Nat. Struct. Biol. 2: 69–76. Siltberg-Liberles, J., and Martinez, A. (2009). Searching distant homologs of the regulatory ACT domain in phenylalanine hydroxylase. Amino Acids 36: 235–249. Sung, T.Y., Chung, T.Y., Hsu, C.P., and Hsieh, M.H. (2011). The ACR11 encodes a novel type of chloroplastic ACT domain repeat protein
1805
that is coordinately expressed with GLN2 in Arabidopsis. BMC Plant Biol. 11: 118. Takabayashi, A., Niwata, A., and Tanaka, A. (2016). Direct interaction with ACR11 is necessary for post-transcriptional control of GLU1-encoded ferredoxin-dependent glutamate synthase in leaves. Sci. Rep. 6: 29668. Zhang, W., Sun, Y., Timofejeva, L., Chen, C., Grossniklaus, U., and Ma, H. (2006). Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133: 3085–3095. Zhu, E., You, C., Wang, S., Cui, J., Niu, B., Wang, Y., Qi, J., Ma, H., and Chang, F. (2015). The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J. 83: 976–990.
LETTER TO THE EDITOR
Reply: The BIF Domain Is Structurally and Functionally Distinct from Other Types of ACT-Like Domains OPEN
We welcome the discussion on the BIF/ACTlike domain in plant bHLH proteins and hope this will help to clarify their functions and structures distinct from those of other types of ACTlike proteins. The bHLH proteins are found in major eukaryotic groups and play important roles in many plant developmental processes and environmental responses (Feller et al., 2006; Pires and Dolan, 2010). The model plant Arabidopsis thaliana has 159 bHLH members; in particular, DYSFUNCTIONAL TAPETUM1 (DYT1) is an early regulator of normal tapetum and pollen development (Zhang et al., 2006; Feng et al., 2012; Zhu et al., 2015). DYT1 expression and function are precisely regulated by a set of interactions: On one hand, protein products of DYT1 downstream genes bHLH010/089/091 interact and form a feedforward loop with DYT1 to control the proper expression of shared downstream anther genes (Zhu et al., 2015); on the other hand, bHLH010/bHLH089/bHLH091 facilitates the stage-dependent nuclear-specific localization of DYT1 in a positive feedback regulatory loop enhancing DYT1 function (Cui et al., 2016). In addition to the bHLH domain, DYT1 and its homologs share a second domain close to its C terminus with a predicted secondary structure of bbabba (a for an a helix and b for a b strand) (Figure 1). This C-terminal domain of DYT1 is required for the interaction with and the nuclear localization by bHLH010/ bHLH089/bHLH091, and transcriptional activation activity and in vivo function of DYT1 (Cui et al., 2016); this domain in DYT1 and homologs was named the BIF domain for bHLH protein interaction and function and also found in over one-third of Arabidopsis bHLH proteins (Cui et al., 2016). Previously, a domain with similar predicted bbabba structure was found in the maize (Zea mays) bHLH transcription factor R and some additional maize and Arabidopsis proteins and was referred to as an ACT-like domain (Feller et al., 2006) or ACT domain (Kong et al., 2012). However, there are substantial functional and OPEN Articles can be viewed without a subscription. www.plantcell.org/cgi/doi/10.1105/tpc.17.00547
structural differences (see below) between the C-terminal BIF/ACT-like domain of plant bHLH proteins (Feller et al., 2006; Kong et al., 2012; Cui et al., 2016) and the original ACT domain and previously reported ACT-like domain in other proteins (Chipman and Shaanan, 2001; Siltberg-Liberles and Martinez, 2009; Lang et al., 2014). The ACT domain and previously reported ACT-like domains are found in functionally diverse proteins. The ACT domain, which was named after the three founding members aspartate kinase, chorismate mutase, and TyrA (prephenate dehydrogenase), is found in a variety of enzymes involved in amino acid and purine metabolism and is known to bind amino acids in negative feedback regulation of such enzymes (Schuller et al., 1995; Aravind and Koonin, 1999; Grant et al., 1999; Chipman and Shaanan, 2001; Grant et al., 2001). The ACT domain was thought to have evolved independently from the catalytic domain of amino acid metabolic enzymes (Hsieh and Goodman, 2002). The ACT domain is found in Arabidopsis amino acid metabolic enzymes such as aspartate kinase, 3-phosphoglycerate dehydrogenase, and acetohydroxyacid synthase regulatory subunit, with suggested regulatory functions (Chipman and Shaanan, 2001; Lee and Duggleby, 2001; Hsieh and Goodman, 2002; Mas-Droux et al., 2006). In addition, the ACT domain is present in ACT domain repeat (ACR) proteins in plants, with multiple members in both Arabidopsis and rice (Oryza sativa), including the OsACR7 and OsACR9, which likely act as the glutamine signal sensors (Hsieh and Goodman, 2002; Hayakawa et al., 2006; Liu, 2006; Kudo et al., 2008; Sung et al., 2011; Takabayashi et al., 2016)). The ACT and ACTlike domains in the regulatory domains of Escherichia coli threonine deaminase have similar babbab secondary structures (Schuller et al., 1995; Aravind and Koonin, 1999; Chipman and Shaanan, 2001; Lang et al., 2014). Another domain was considered to be an ACT-like domain because of a predicted babbab secondary structure similar to that of ACT-proteins, but it was named RAM, for regulation of amino acid metabolism (Ettema et al., 2002).
By contrast, the BIF/ACT-like domains in plant bHLH proteins are predicted to share a bbabba structure, which differs from the babbab structure in the position of four out ofsix motifs (Felleretal., 2006;Kongetal., 2012; Cui et al., 2016). At the sequence level, there are very low levels of amino acid sequence identities, with only 4.6% between the ACT domain of3-phosphoglyceratedehydrogenaseandthe ACT-like domain of threonine deaminase, and only 6.6% between the ACT domain and the ACT-like RAM domain; these percentages are not statistically different from that between two random sequences. The levels of amino acid sequence identities between the ACT-like domains in plant bHLH proteins and the ACT domains are also very low, such that the DYT1 and R proteins are not found in the Pfam database as having an ACT-like domain. In short, the “ACT-like domain” is a general termforvariousdomainsthatshowsimilarstructural similarities to the ACT domain, whereas the “BIF domain” is a more specific term referring to those in DYT1 and other plant bHLH proteins with distinct function in dimerization and nuclear localization of interacting proteins and the bbabba topology. We consider the domain in plant bHLH proteins sufficiently different from others to warrant a distinct name. Fang Chang,a Jie Cui,a Linbo Wang,a and Hong Maa ,b ,1 a State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering and Institute of Biodiversity Sciences, Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200433, China b Center for Evolutionary Biology, Institutes of Biomedical Sciences, Fudan University, Shanghai 200433, China 1 Address
correspondence to hxm16@psu. edu.
ORCID ID: 0000-0001-8717-4422 (H.M.)
1804
The Plant Cell
Figure 1. The Location and Position (with P Value) of DYT1 Orthologs: Conserved Motifs in the DYT1 Sequence. (A) A schematic diagram representing the a-helices (magenta box) and b-sheets (green arrows) in DYT1. (B) A block diagram showing the eight best nonoverlapping tiling of motifs from the analysis of the DYT1 amino acid sequences and those of 54 DYT1 orthologs; the conserved motifs (M1;M8) are indicated as boxes with different colors. The length of each motif is relative to the length of DYT1 sequence, and the height of each box provides an indication of the significance of the match. (C) The location and amino acid sequences of each motif. Position P value (the probability of a single random subsequence of the length of the motif scoring at least as well as the observed match) is indicated above each motif. The secondary structure of DYT1 was predicted on the website https://www. predictprotein.org, and the motif analysis was performed using MEME software (Bailey and Elkan, 1994).
ACKNOWLEDGMENTS The BIF domain-related work was supported by grants from the Ministry of Science and Technology (2012CB910503) and the National Science Foundation of China (31130006 and 31070274). AUTHOR CONTRIBUTIONS F.C. and J.C. drafted an early version of the manuscript. F.C. prepared a new version of the manuscript with sequence analyses by L.W. H.M. discussed the manuscript with other authors and revised the manuscript. Received July 10, 2017; revised June 10, 2017; accepted July 26, 2017; published July 26, 2017.
REFERENCES Aravind, L., and Koonin, E.V. (1999). Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches. J. Mol. Biol. 287: 1023–1040. Bailey, T.L., and Elkan, C. (1994). Fitting a mixture model by expectation maximization
to discover motifs in biopolymers. University of California San Diego Technical Report CS94–351. Chipman, D.M., and Shaanan, B. (2001). The ACT domain family. Curr. Opin. Struct. Biol. 11: 694–700. Cui, J., You, C., Zhu, E., Huang, Q., Ma, H., and Chang, F. (2016). Feedback regulation of DYT1 by interactions with downstream bHLH factors promotes DYT1 nuclear localization and anther development. Plant Cell 28: 1078– 1093. Ettema, T.J.G., Brinkman, A.B., Tani, T.H., Rafferty, J.B., and Van Der Oost, J. (2002). A novel ligand-binding domain involved in regulation of amino acid metabolism in prokaryotes. J. Biol. Chem. 277: 37464–37468. Feller, A., Hernandez, J.M., and Grotewold, E. (2006). An ACT-like domain participates in the dimerization of several plant basic-helix-loophelix transcription factors. J. Biol. Chem. 281: 28964–28974. Feng, B., Lu, D., Ma, X., Peng, Y., Sun, Y., Ning, G., and Ma, H. (2012). Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J. 72: 612–624.
Grant, G.A., Hu, Z., and Xu, X.L. (2001). Specific interactions at the regulatory domain-substrate binding domain interface influence the cooperativity of inhibition and effector binding in Escherichia coli D-3-phosphoglycerate dehydrogenase. J. Biol. Chem. 276: 1078– 1083. Grant, G.A., Kim, S.J., Xu, X.L., and Hu, Z. (1999). The contribution of adjacent subunits to the active sites of D-3-phosphoglycerate dehydrogenase. J. Biol. Chem. 274: 5357–5361. Hayakawa, T., Kudo, T., Ito, T., Takahashi, N., and Yamaya, T. (2006). ACT domain repeat protein 7, ACR7, interacts with a chaperone HSP18.0-CII in rice nuclei. Plant Cell Physiol. 47: 891–904. Hsieh, M.H., and Goodman, H.M. (2002). Molecular characterization of a novel gene family encoding ACT domain repeat proteins in Arabidopsis. Plant Physiol. 130: 1797–1806. Kong, Q., Pattanaik, S., Feller, A., Werkman, J.R., Chai, C., Wang, Y., Grotewold, E., and Yuan, L. (2012). Regulatory switch enforced by basic helix-loop-helix and ACT-domain mediated dimerizations of the maize transcription factor R. Proc. Natl. Acad. Sci. USA 109: E2091–E2097.
August 2017
Kudo, T., Kawai, A., Yamaya, T., and Hayakawa, T. (2008). Cellular distribution of ACT domain repeat protein 9, a nuclear localizing protein, in rice (Oryza sativa). Physiol. Plant. 133: 167–179. Lang, E.J., Cross, P.J., Mittelsta¨dt, G., Jameson, G.B., and Parker, E.J. (2014). Allosteric ACTion: the varied ACT domains regulating enzymes of amino-acid metabolism. Curr. Opin. Struct. Biol. 29: 102–111. Lee, Y.T., and Duggleby, R.G. (2001). Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry 40: 6836–6844. Liu, Q. (2006). Computational identification and systematic analysis of the ACR gene family in Oryza sativa. J. Plant Physiol. 163: 445–451. Mas-Droux, C., Curien, G., Robert-Genthon, M., Laurencin, M., Ferrer, J.L., and Dumas,
R. (2006). A novel organization of ACT domains in allosteric enzymes revealed by the crystal structure of Arabidopsis aspartate kinase. Plant Cell 18: 1681–1692. Pires, N., and Dolan, L. (2010). Origin and diversification of basic-helix-loop-helix proteins in plants. Mol. Biol. Evol. 27: 862–874. Schuller, D.J., Grant, G.A., and Banaszak, L.J. (1995). The allosteric ligand site in the Vmax-type cooperative enzyme phosphoglycerate dehydrogenase. Nat. Struct. Biol. 2: 69–76. Siltberg-Liberles, J., and Martinez, A. (2009). Searching distant homologs of the regulatory ACT domain in phenylalanine hydroxylase. Amino Acids 36: 235–249. Sung, T.Y., Chung, T.Y., Hsu, C.P., and Hsieh, M.H. (2011). The ACR11 encodes a novel type of chloroplastic ACT domain repeat protein
1805
that is coordinately expressed with GLN2 in Arabidopsis. BMC Plant Biol. 11: 118. Takabayashi, A., Niwata, A., and Tanaka, A. (2016). Direct interaction with ACR11 is necessary for post-transcriptional control of GLU1-encoded ferredoxin-dependent glutamate synthase in leaves. Sci. Rep. 6: 29668. Zhang, W., Sun, Y., Timofejeva, L., Chen, C., Grossniklaus, U., and Ma, H. (2006). Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133: 3085–3095. Zhu, E., You, C., Wang, S., Cui, J., Niu, B., Wang, Y., Qi, J., Ma, H., and Chang, F. (2015). The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J. 83: 976–990.
