The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in Arabidopsis
To reveal the mechanisms underlying root adaptation to drought stress, we isolated and characterized an Arabidopsis mutant, <i>dig5</i> (<i>d</i>rought <i>i</i>nhibition of lateral root <i>g</i>rowth <i>5</i>), which exhibited increased sen...
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MDPI AG
2022-09-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/18/10642 |
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| author | Wei Liu Tao Chen Yajie Liu Quang Tri Le Ruigang Wang Hojoung Lee Liming Xiong |
| author_facet | Wei Liu Tao Chen Yajie Liu Quang Tri Le Ruigang Wang Hojoung Lee Liming Xiong |
| author_sort | Wei Liu |
| collection | DOAJ |
| description | To reveal the mechanisms underlying root adaptation to drought stress, we isolated and characterized an Arabidopsis mutant, <i>dig5</i> (<i>d</i>rought <i>i</i>nhibition of lateral root <i>g</i>rowth <i>5</i>), which exhibited increased sensitivity to the phytohormone abscisic acid (ABA) for the inhibition of lateral root growth. The <i>dig5</i> mutant also had fewer lateral roots under normal conditions and the aerial parts were yellowish with a lower level of chlorophylls. The mutant seedlings also displayed phenotypes indicative of impaired auxin transport, such as abnormal root curling, leaf venation defects, absence of apical hook formation, and reduced hypocotyl elongation in darkness. Auxin transport assays with [<sup>3</sup>H]-labeled indole acetic acid (IAA) confirmed that <i>dig5</i> roots were impaired in polar auxin transport. Map-based cloning and complementation assays indicated that the <i>DIG5</i> locus encodes a chloroplast-localized tRNA adenosine deaminase arginine (TADA) that is involved in chloroplast protein translation. The levels of flavonoids, which are naturally occurring auxin transport inhibitors in plants, were significantly higher in <i>dig5</i> roots than in the wild type roots. Further investigation showed that flavonoid biosynthetic genes were upregulated in <i>dig5</i>. Introduction of the flavonoid biosynthetic mutation <i>transparent testa 4</i> (<i>tt4)</i> into <i>dig5</i> restored the lateral root growth of <i>dig5</i>. Our study uncovers an important role of DIG5/TADA in retrogradely controlling flavonoid biosynthesis and lateral root development. We suggest that the DIG5-related signaling pathways, triggered likely by drought-induced chlorophyll breakdown and leaf senescence, may potentially help the plants to adapt to drought stress through optimizing the root system architecture. |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-1fc936838c5f4c48b29fb0dc4011b9062023-11-23T16:45:30ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-09-0123181064210.3390/ijms231810642The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in ArabidopsisWei Liu0Tao Chen1Yajie Liu2Quang Tri Le3Ruigang Wang4Hojoung Lee5Liming Xiong6Donald Danforth Plant Science Center, St. Louis, MO 63132, USACollege of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, ChinaDepartment of Biology, Hong Kong Baptist University, Kowloon Tang, Hong Kong, ChinaDepartment of Plant Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul 136-713, KoreaDonald Danforth Plant Science Center, St. Louis, MO 63132, USADepartment of Plant Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul 136-713, KoreaDonald Danforth Plant Science Center, St. Louis, MO 63132, USATo reveal the mechanisms underlying root adaptation to drought stress, we isolated and characterized an Arabidopsis mutant, <i>dig5</i> (<i>d</i>rought <i>i</i>nhibition of lateral root <i>g</i>rowth <i>5</i>), which exhibited increased sensitivity to the phytohormone abscisic acid (ABA) for the inhibition of lateral root growth. The <i>dig5</i> mutant also had fewer lateral roots under normal conditions and the aerial parts were yellowish with a lower level of chlorophylls. The mutant seedlings also displayed phenotypes indicative of impaired auxin transport, such as abnormal root curling, leaf venation defects, absence of apical hook formation, and reduced hypocotyl elongation in darkness. Auxin transport assays with [<sup>3</sup>H]-labeled indole acetic acid (IAA) confirmed that <i>dig5</i> roots were impaired in polar auxin transport. Map-based cloning and complementation assays indicated that the <i>DIG5</i> locus encodes a chloroplast-localized tRNA adenosine deaminase arginine (TADA) that is involved in chloroplast protein translation. The levels of flavonoids, which are naturally occurring auxin transport inhibitors in plants, were significantly higher in <i>dig5</i> roots than in the wild type roots. Further investigation showed that flavonoid biosynthetic genes were upregulated in <i>dig5</i>. Introduction of the flavonoid biosynthetic mutation <i>transparent testa 4</i> (<i>tt4)</i> into <i>dig5</i> restored the lateral root growth of <i>dig5</i>. Our study uncovers an important role of DIG5/TADA in retrogradely controlling flavonoid biosynthesis and lateral root development. We suggest that the DIG5-related signaling pathways, triggered likely by drought-induced chlorophyll breakdown and leaf senescence, may potentially help the plants to adapt to drought stress through optimizing the root system architecture.https://www.mdpi.com/1422-0067/23/18/10642lateral rootsroot system architectureflavonoidpolar auxin transportchloroplastretrograde signaling |
| spellingShingle | Wei Liu Tao Chen Yajie Liu Quang Tri Le Ruigang Wang Hojoung Lee Liming Xiong The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in Arabidopsis International Journal of Molecular Sciences lateral roots root system architecture flavonoid polar auxin transport chloroplast retrograde signaling |
| title | The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in Arabidopsis |
| title_full | The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in Arabidopsis |
| title_fullStr | The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in Arabidopsis |
| title_full_unstemmed | The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in Arabidopsis |
| title_short | The Plastidial DIG5 Protein Affects Lateral Root Development by Regulating Flavonoid Biosynthesis and Auxin Transport in Arabidopsis |
| title_sort | plastidial dig5 protein affects lateral root development by regulating flavonoid biosynthesis and auxin transport in arabidopsis |
| topic | lateral roots root system architecture flavonoid polar auxin transport chloroplast retrograde signaling |
| url | https://www.mdpi.com/1422-0067/23/18/10642 |
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