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Mobile PEAR transcription factors integrate hormone and miRNA cues to prime cambial growth

ABSTRACT: In addition to apical growth, plants undergo radial growth to increase girth, a particularly prominent feature in trees. During both apical and radial growth the phytohormones auxin and cytokinins form symmetries that govern further growth patterns. But whereas the gene regulatory networks interpreting the hormonal fields during apical growth are well established, such networks are not known for the radial growth. We show here that the initiation of radial growth occurs around early protophloem sieve element (PSE) cell files of the root procambial tissue in Arabidopsis. In this domain cytokinin signalling promotes expression of a pair of novel mobile transcription factors, PHLOEM EARLY DOF (PEAR1, PEAR2) and their four homologs (OBP2, DOF6, TMO6 and HCA2), collectively called PEAR proteins. The PEAR proteins form a short-range concentration gradient peaking at PSE and activating gene expression that promotes radial growth. The expression and function of PEAR proteins are antagonized by well-established polarity transcription factors, HD-ZIP III, whose expression is concentrated in the more internal domain of radially non-dividing procambial cells by the function of auxin and mobile miR165/166. The PEAR proteins locally promote transcription of their inhibitory HD-ZIP III genes, thereby establishing a negative feedback loop that forms a sharp boundary demarking the zone of cell divisions. Taken together, we have established a network, in which the PEAR - HD-ZIP III module integrates the spatial information of the hormonal domains and miRNA gradients during root procambial development, to provide a pre-pattern with actively dividing and more quiescent zones, thus priming radial growth.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE115183 | GEO | 2018/11/09

REPOSITORIES: GEO

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Project description:The class III HD-ZIP transcription factors regulate vascular patterning in Arabidopsis thaliana roots. In this expression study we compare the expression profile of the athb8 cna phb phv quadruple mutant to its wild type. The results are presented in PHABULOSA mediates an auxin signaling loop to regulate vascular patterning in Arabidopsis by Christina Joy Müller, Ana Elisa Valdés, Guodong Wang, Prashanth Ramachandran, Lisa Beste, Daniel Uddenberg, and Annelie Carlsbecker, accepted for publication in Plant Physiology Nov. 2015. Plant vascular tissues, xylem and phloem, differentiate in distinct patterns from procambial cells as an integral transport system for water, sugars and signaling molecules. Procambium formation is promoted by high auxin levels activating class III homeodomain leucine zipper (HD-ZIP III) transcription factors (TFs). In the root of Arabidopsis thaliana, HD-ZIP III TFs dose-dependently govern the patterning of the xylem axis, with higher levels promoting metaxylem cell identity in the central axis and lower levels protoxylem at its flanks. It is, however, unclear by what mechanisms the HD-ZIP III TFs control xylem axis patterning. Here we present data suggesting that an important mechanism is their ability to moderate auxin response. We found that changes in HD-ZIP III TF levels affect the expression of genes encoding core auxin response molecules. We show that one of the HD-ZIP III TFs, PHABULOSA, directly binds the promoter of both MONOPTEROS/AUXIN RESPONSE FACTOR5 (MP/ARF5), a key factor in vascular formation, and IAA20, encoding an AUX/IAA protein which is stable in the presence of auxin and able to interact with and repress MP activity. The double mutant of IAA20 and its closest homologue IAA30 forms ectopic protoxylem, while overexpression of IAA30 causes discontinuous protoxylem and occasional ectopic metaxylem, similar to a weak loss-of-function mp-mutant. Our results provide evidence that HD-ZIP III TFs directly affect auxin response and mediate a feed forward loop formed by MP and IAA20 that may focus and stabilize auxin response during vascular patterning and differentiation of xylem cell types.

Project description:The class III HD-ZIPtranscription factors regulate vascular patterning in Arabidopsis thaliana roots. In this expression study we compare the expression profile in root tips upon miR165 induction, after 6h, 10h and 24h. The results are presented in PHABULOSA mediates an auxin signaling loop to regulate vascular patterning in Arabidopsis by Christina Joy Müller, Ana Elisa Valdés, Guodong Wang, Prashanth Ramachandran, Lisa Beste, Daniel Uddenberg, and Annelie Carlsbecker, accepted for publication in Plant Physiology Nov. 2015. Plant vascular tissues, xylem and phloem, differentiate in distinct patterns from procambial cells as an integral transport system for water, sugars and signaling molecules. Procambium formation is promoted by high auxin levels activating class III homeodomain leucine zipper (HD-ZIP III) transcription factors (TFs). In the root of Arabidopsis thaliana, HD-ZIP III TFs dose-dependently govern the patterning of the xylem axis, with higher levels promoting metaxylem cell identity in the central axis and lower levels protoxylem at its flanks. It is, however, unclear by what mechanisms the HD-ZIP III TFs control xylem axis patterning. Here we present data suggesting that an important mechanism is their ability to moderate auxin response. We found that changes in HD-ZIP III TF levels affect the expression of genes encoding core auxin response molecules. We show that one of the HD-ZIP III TFs, PHABULOSA, directly binds the promoter of both MONOPTEROS/AUXIN RESPONSE FACTOR5 (MP/ARF5), a key factor in vascular formation, and IAA20, encoding an AUX/IAA protein which is stable in the presence of auxin and able to interact with and repress MP activity. The double mutant of IAA20 and its closest homologue IAA30 forms ectopic protoxylem, while overexpression of IAA30 causes discontinuous protoxylem and occasional ectopic metaxylem, similar to a weak loss-of-function mp-mutant. Our results provide evidence that HD-ZIP III TFs directly affect auxin response and mediate a feed forward loop formed by MP and IAA20 that may focus and stabilize auxin response during vascular patterning and differentiation of xylem cell types.

Project description:The class III HD-ZIP transcription factors regulate vascular patterning in Arabidopsis thaliana roots. In this expression study we compare the expression profile of the cna-2 phb-13 phv-11 and cna-2 phb-13 phv-11 rev-6 mutants to their wild type. The results are presented in PHABULOSA mediates an auxin signaling loop to regulate vascular patterning in Arabidopsis by Christina Joy Müller, Ana Elisa Valdés, Guodong Wang, Prashanth Ramachandran, Lisa Beste, Daniel Uddenberg, and Annelie Carlsbecker, accepted for publication in Plant Physiology Nov. 2015. Plant vascular tissues, xylem and phloem, differentiate in distinct patterns from procambial cells as an integral transport system for water, sugars and signaling molecules. Procambium formation is promoted by high auxin levels activating class III homeodomain leucine zipper (HD-ZIP III) transcription factors (TFs). In the root of Arabidopsis thaliana, HD-ZIP III TFs dose-dependently govern the patterning of the xylem axis, with higher levels promoting metaxylem cell identity in the central axis and lower levels protoxylem at its flanks. It is, however, unclear by what mechanisms the HD-ZIP III TFs control xylem axis patterning. Here we present data suggesting that an important mechanism is their ability to moderate auxin response. We found that changes in HD-ZIP III TF levels affect the expression of genes encoding core auxin response molecules. We show that one of the HD-ZIP III TFs, PHABULOSA, directly binds the promoter of both MONOPTEROS/AUXIN RESPONSE FACTOR5 (MP/ARF5), a key factor in vascular formation, and IAA20, encoding an AUX/IAA protein which is stable in the presence of auxin and able to interact with and repress MP activity. The double mutant of IAA20 and its closest homologue IAA30 forms ectopic protoxylem, while overexpression of IAA30 causes discontinuous protoxylem and occasional ectopic metaxylem, similar to a weak loss-of-function mp-mutant. Our results provide evidence that HD-ZIP III TFs directly affect auxin response and mediate a feed forward loop formed by MP and IAA20 that may focus and stabilize auxin response during vascular patterning and differentiation of xylem cell types.

Project description:Background The homeodomain leucine zipper (HD-Zip) transcription factor family is one of the largest plant specific superfamilies, and includes genes with roles in modulation of plant growth and response to environmental stresses. Many HD-Zip genes are characterized in Arabidopsis (Arabidopsis thaliana), and members of the family are being investigated for abiotic stress responses in rice (Oryza sativa), maize (Zea mays), poplar (Populus trichocarpa) and cucumber (Cucmis sativus). Findings in these species suggest HD-Zip genes as high priority candidates for crop improvement. Results In this study we have identified members of the HD-Zip gene family in soybean cv. 'Williams 82', and characterized their expression under dehydration and salt stress. Homology searches with BLASTP and Hidden Markov Model guided sequence alignments identified 101 HD-Zip genes in the soybean genome. Phylogeny reconstruction coupled with domain and gene structure analyses using soybean, Arabidopsis, rice, grape (Vitis vinifera), and Medicago truncatula homologues enabled placement of these sequences into four previously described subfamilies. Of the 101 HD-Zip genes identified in soybean, 88 exist as whole-genome duplication-derived gene pairs, indicating high retention of these genes following polyploidy in Glycine ~10 Mya. The HD-Zip genes exhibit ubiquitous expression patterns across 24 conditions that include 17 tissues of soybean. An RNA-Seq experiment performed to study differential gene expression at 0, 1, 6 and 12 hr soybean roots under dehydration and salt stress identified 20 differentially expressed (DE) genes. Several of these DE genes are orthologs of genes previously reported to play a role under abiotic stress, implying conservation of HD-Zip gene functions across species. Screening of HD-Zip promoters identified transcription factor binding sites that are overrepresented in the DE genes under both dehydration and salt stress, providing further support for the role of HD-Zip genes in abiotic stress responses. Conclusions We provide a thorough description of soybean HD-Zip genes, and identify potential candidates with probable roles in dehydration and salt stress. Expression profiles generated for all soybean genes, under dehydration and salt stress, at four time points, will serve as an important resource for the soybean research community, and will aid in understanding plant responses to abiotic stress.

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Mobile PEAR transcription factors integrate hormone and miRNA cues to prime cambial growth

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