Publications by authors named "Hitoshi Sakakibara"

258 Publications

Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana.

Nat Commun 2021 08 16;12(1):4944. Epub 2021 Aug 16.

Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi, Japan.

Plants use nitrate, ammonium, and organic nitrogen in the soil as nitrogen sources. Since the elevated CO environment predicted for the near future will reduce nitrate utilization by C species, ammonium is attracting great interest. However, abundant ammonium nutrition impairs growth, i.e., ammonium toxicity, the primary cause of which remains to be determined. Here, we show that ammonium assimilation by GLUTAMINE SYNTHETASE 2 (GLN2) localized in the plastid rather than ammonium accumulation is a primary cause for toxicity, which challenges the textbook knowledge. With exposure to toxic levels of ammonium, the shoot GLN2 reaction produced an abundance of protons within cells, thereby elevating shoot acidity and stimulating expression of acidic stress-responsive genes. Application of an alkaline ammonia solution to the ammonium medium efficiently alleviated the ammonium toxicity with a concomitant reduction in shoot acidity. Consequently, we conclude that a primary cause of ammonium toxicity is acidic stress.
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http://dx.doi.org/10.1038/s41467-021-25238-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8367978PMC
August 2021

Identification of the unique molecular framework of heterophylly in the amphibious plant Callitriche palustris L.

Plant Cell 2021 Jul 27. Epub 2021 Jul 27.

Graduate School of Science, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.

Heterophylly is the development of different leaf forms in a single plant depending on the environmental conditions. It is often observed in amphibious aquatic plants that can grow under both aerial and submerged conditions. Although heterophylly is well recognized in aquatic plants, the associated developmental mechanisms and the molecular basis remain unclear. To clarify these underlying developmental and molecular mechanisms, we analyzed heterophyllous leaf formation in an aquatic plant, Callitriche palustris. Morphological analyses revealed extensive cell elongation and the rearrangement of cortical microtubules in the elongated submerged leaves of C. palustris. Our observations also suggested that gibberellin, ethylene, and abscisic acid all regulate the formation of submerged leaves. However, the perturbation of one or more of the hormones was insufficient to induce the formation of submerged leaves under aerial conditions. Finally, we analyzed gene expression changes during aerial and submerged leaf development and narrowed down the candidate genes controlling heterophylly via transcriptomic comparisons, including a comparison with a closely related terrestrial species. We discovered that the molecular mechanism regulating heterophylly in C. palustris is associated with hormonal changes and diverse transcription factor gene expression profiles, suggesting differences from the corresponding mechanisms in previously investigated amphibious plants.
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http://dx.doi.org/10.1093/plcell/koab192DOI Listing
July 2021

Alterations in hormonal signals spatially coordinate distinct responses to DNA double-strand breaks in roots.

Sci Adv 2021 Jun 16;7(25). Epub 2021 Jun 16.

Graduate School of Science and Technology, Nara Institute of Science and Technology, Takayama 8916-5, Ikoma, Nara 630-0192, Japan.

Plants have a high ability to cope with changing environments and grow continuously throughout life. However, the mechanisms by which plants strike a balance between stress response and organ growth remain elusive. Here, we found that DNA double-strand breaks enhance the accumulation of cytokinin hormones through the DNA damage signaling pathway in the root tip. Our data showed that activation of cytokinin signaling suppresses the expression of some of the genes that encode efflux carriers of another hormone, auxin, thereby decreasing the auxin signals in the root tip and causing cell cycle arrest at G phase and stem cell death. Elevated cytokinin signaling also promotes an early transition from cell division to endoreplication in the basal part of the root apex. We propose that plant hormones spatially coordinate differential DNA damage responses, thereby maintaining genome integrity and minimizing cell death to ensure continuous root growth.
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http://dx.doi.org/10.1126/sciadv.abg0993DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8208723PMC
June 2021

Nitrogen Nutrition Promotes Rhizome Bud Outgrowth via Regulation of Cytokinin Biosynthesis Genes and an Ortholog of .

Front Plant Sci 2021 30;12:670101. Epub 2021 Apr 30.

RIKEN Center for Sustainable Resource Science, Yokohama, Japan.

, a wild rice, can propagate vegetatively via rhizome formation and, thereby, expand its territory through horizontal growth of branched rhizomes. The structural features of rhizomes are similar to those of aerial stems; however, the physiological roles of the two organs are different. Nitrogen nutrition is presumed to be linked to the vegetative propagation activity of rhizomes, but the regulation of rhizome growth in response to nitrogen nutrition and the underlying biological processes have not been well characterized. In this study, we analyzed rhizome axillary bud growth in response to nitrogen nutrition and examined the involvement of cytokinin-mediated regulation in the promotion of bud outgrowth in . Our results showed that nitrogen nutrition sufficiency promoted rhizome bud outgrowth to form secondary rhizomes. In early stages of the response to nitrogen application, glutamine accumulated rapidly, two cytokinin biosynthesis genes, isopentenyltransferase, and , were up-regulated with accompanying cytokinin accumulation, and expression of an ortholog of , a negative regulator of axillary bud outgrowth, was severely repressed in rhizomes. These results suggest that, despite differences in physiological roles of these organs, the nitrogen-dependent outgrowth of rhizome axillary buds in is regulated by a mechanism similar to that of shoot axillary buds in Our findings provide a clue for understanding how branched rhizome growth is regulated to enhance nutrient acquisition strategies.
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http://dx.doi.org/10.3389/fpls.2021.670101DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8120282PMC
April 2021

Gene expression evolution in pattern-triggered immunity within Arabidopsis thaliana and across Brassicaceae species.

Plant Cell 2021 Mar 5. Epub 2021 Mar 5.

State Key Laboratory of Agricultural Microbiology, Interdisciplinary Science Research Institute, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China.

Plants recognize surrounding microbes by sensing microbe-associated molecular patterns (MAMPs) to activate pattern-triggered immunity (PTI). Despite their significance for microbial control, the evolution of PTI responses remains largely uncharacterized. Here, by employing comparative transcriptomics of six Arabidopsis thaliana accessions and three additional Brassicaceae species to investigate PTI responses, we identified a set of genes that commonly respond to the MAMP flg22 and genes that exhibit species-specific expression signatures. Variation in flg22-triggered transcriptome responses across Brassicaceae species was incongruent with their phylogeny, while expression changes were strongly conserved within A. thaliana. We found the enrichment of WRKY transcription factor binding sites in the 5'-regulatory regions of conserved and species-specific responsive genes, linking the emergence of WRKY-binding sites with the evolution of gene expression patterns during PTI. Our findings advance our understanding of the evolution of the transcriptome during biotic stress.
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http://dx.doi.org/10.1093/plcell/koab073DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8290292PMC
March 2021

Acetic-acid-induced jasmonate signaling in root enhances drought avoidance in rice.

Sci Rep 2021 03 18;11(1):6280. Epub 2021 Mar 18.

Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, 305-8602, Japan.

Conferring drought resistant traits to crops is one of the major aims of current breeding programs in response to global climate changes. We previously showed that exogenous application of acetic acid to roots of various plants could induce increased survivability under subsequent drought stress conditions, but details of the metabolism of exogenously applied acetic acid, and the nature of signals induced by its application, have not been unveiled. In this study, we show that rice rapidly induces jasmonate signaling upon application of acetic acid, resulting in physiological changes similar to those seen under drought. The major metabolite of the exogenously applied acetic acid in xylem sap was determined as glutamine-a common and abundant component of xylem sap-indicating that acetic acid is not the direct agent inducing the observed physiological responses in shoots. Expression of drought-responsive genes in shoot under subsequent drought conditions was attenuated by acetic acid treatment. These data suggest that acetic acid activates root-to-shoot jasmonate signals that partially overlap with those induced by drought, thereby conferring an acclimated state on shoots prior to subsequent drought.
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http://dx.doi.org/10.1038/s41598-021-85355-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7973560PMC
March 2021

Nitrate-Dependent Modulation of Root System Architecture in Maize: A Balance between Strigolactone and Auxin Pathways.

Plant Cell Physiol 2021 Sep;62(4):541-542

Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601 Japan.

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http://dx.doi.org/10.1093/pcp/pcab032DOI Listing
September 2021

Plant stem cell research is uncovering the secrets of longevity and persistent growth.

Plant J 2021 04 25;106(2):326-335. Epub 2021 Mar 25.

Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601, Japan.

Plant stem cells have several extraordinary features: they are generated de novo during development and regeneration, maintain their pluripotency, and produce another stem cell niche in an orderly manner. This enables plants to survive for an extended period and to continuously make new organs, representing a clear difference in their developmental program from animals. To uncover regulatory principles governing plant stem cell characteristics, our research project 'Principles of pluripotent stem cells underlying plant vitality' was launched in 2017, supported by a Grant-in-Aid for Scientific Research on Innovative Areas from the Japanese government. Through a collaboration involving 28 research groups, we aim to identify key factors that trigger epigenetic reprogramming and global changes in gene networks, and thereby contribute to stem cell generation. Pluripotent stem cells in the shoot apical meristem are controlled by cytokinin and auxin, which also play a crucial role in terminating stem cell activity in the floral meristem; therefore, we are focusing on biosynthesis, metabolism, transport, perception, and signaling of these hormones. Besides, we are uncovering the mechanisms of asymmetric cell division and of stem cell death and replenishment under DNA stress, which will illuminate plant-specific features in preserving stemness. Our technology support groups expand single-cell omics to describe stem cell behavior in a spatiotemporal context, and provide correlative light and electron microscopic technology to enable live imaging of cell and subcellular dynamics at high spatiotemporal resolution. In this perspective, we discuss future directions of our ongoing projects and related research fields.
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http://dx.doi.org/10.1111/tpj.15184DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8252613PMC
April 2021

Difference Between Day and Night Temperatures Affects Stem Elongation in Tomato () Seedlings via Regulation of Gibberellin and Auxin Synthesis.

Front Plant Sci 2020 8;11:577235. Epub 2020 Dec 8.

RIKEN Center for Sustainable Resource Science, Yokohama, Japan.

Temperature is a critical environmental factor governing plant growth and development. The difference between day temperature (DT) and night temperature (NT), abbreviated as DIF, influences plant architecture. Subjecting plants to artificial DIF treatments is an effective strategy in ornamental horticulture. For example, negative DIF (when DT - NT < 0) generally inhibits stem elongation, resulting in dwarf plants. However, the mechanisms underlying stem growth regulation by DIF remains to be completely elucidated. In this study, we aimed to analyze the growth, transcriptome, and phytohormone profiles of tomato () seedlings grown under different DIF treatments. Under positive DIF (when DT - NT > 0), in contrast to the control temperature (25°C/20°C, DT/NT), high temperature (30°C/25°C) increased stem length and thickness, as well as the number of xylem vessels. Conversely, compared with the positive high temperature DIF treatment (30°C/25°C), under negative DIF treatment (25°C/30°C) stem elongation was inhibited, but stem thickness and the number of xylem vessels were not affected. The negative DIF treatment decreased the expression of gibberellin (GA)-, auxin-, and cell wall-related genes in the epicotyl, as well as the concentrations of GAs and indole-3-acetic acid (IAA). The expression of these genes and concentrations of these hormones increased under high temperature compared to those under the control temperature positive DIF. Our results suggest that stem length in tomato seedlings is controlled by changes in GA and IAA biosynthesis in response to varying day and night temperatures.
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http://dx.doi.org/10.3389/fpls.2020.577235DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7752778PMC
December 2020

Endogenous gibberellins affect root nodule symbiosis via transcriptional regulation of NODULE INCEPTION in Lotus japonicus.

Plant J 2021 03 9;105(6):1507-1520. Epub 2021 Jan 9.

Graduate School of Science and Technology, Kwansei Gakuin University, 2-1 Gakuen, Sanda, Hyogo, 669-1337, Japan.

Legumes and nitrogen-fixing rhizobial bacteria establish root nodule symbiosis, which is orchestrated by several plant hormones. Exogenous addition of biologically active gibberellic acid (GA) is known to inhibit root nodule symbiosis. However, the precise role of GA has not been elucidated because of the trace amounts of these hormones in plants and the multiple functions of GAs. Here, we found that GA signaling acts as a key regulator in a long-distance negative-feedback system of root nodule symbiosis called autoregulation of nodulation (AON). GA biosynthesis is activated during nodule formation in and around the nodule vascular bundles, and bioactive GAs accumulate in the nodule. In addition, GA signaling induces expression of the symbiotic transcription factor NODULE INCEPTION (NIN) via a cis-acting region on the NIN promoter. Mutants with deletions of this cis-acting region have increased susceptibility to rhizobial infection and reduced GA-induced CLE-RS1 and CLE-RS2 expression, suggesting that the inhibitory effect of GAs occurs through AON. This is supported by the GA-insensitive phenotypes of an AON-defective mutant of HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) and a reciprocal grafting experiment. Thus, endogenous GAs induce NIN expression via its GA-responsive cis-acting region, and subsequently the GA-induced NIN activates the AON system to regulate nodule formation.
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http://dx.doi.org/10.1111/tpj.15128DOI Listing
March 2021

Molecular and Biochemical Differences in Leaf Explants and the Implication for Regeneration Ability in (Brassicaceae).

Plants (Basel) 2020 Oct 15;9(10). Epub 2020 Oct 15.

Faculty of Life Sciences, Kyoto Sangyo University, Kyoto 603-8555, Japan.

Plants have a high regeneration capacity and some plant species can regenerate clone plants, called plantlets, from detached vegetative organs. We previously outlined the molecular mechanisms underlying plantlet regeneration from (Brassicaceae) leaf explants. However, the fundamental difference between the plant species that can and cannot regenerate plantlets from vegetative organs remains unclear. Here, we hypothesized that the viability of leaf explants is a key factor affecting the regeneration capacity of . To test this hypothesis, the viability of and leaf explants were compared, with respect to the maintenance of photosynthetic activity, senescence, and immune response. Time-course analyses of photosynthetic activity revealed that leaf explants can survive longer than those of . Endogenous abscisic acid (ABA) and jasmonic acid (JA) were found at low levels in leaf explant of . Time-course transcriptome analysis of and leaf explants suggested that senescence was suppressed at the transcriptional level in . Application of exogenous ABA reduced the efficiency of plantlet regeneration. Overall, our results propose that in nature, plant species that can regenerate in nature can survive for a long time.
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http://dx.doi.org/10.3390/plants9101372DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7602576PMC
October 2020

A genome resource for green millet Setaria viridis enables discovery of agronomically valuable loci.

Nat Biotechnol 2020 10 5;38(10):1203-1210. Epub 2020 Oct 5.

Donald Danforth Plant Science Center, St. Louis, MO, USA.

Wild and weedy relatives of domesticated crops harbor genetic variants that can advance agricultural biotechnology. Here we provide a genome resource for the wild plant green millet (Setaria viridis), a model species for studies of C grasses, and use the resource to probe domestication genes in the close crop relative foxtail millet (Setaria italica). We produced a platinum-quality genome assembly of S. viridis and de novo assemblies for 598 wild accessions and exploited these assemblies to identify loci underlying three traits: response to climate, a 'loss of shattering' trait that permits mechanical harvest and leaf angle, a predictor of yield in many grass crops. With CRISPR-Cas9 genome editing, we validated Less Shattering1 (SvLes1) as a gene whose product controls seed shattering. In S. italica, this gene was rendered nonfunctional by a retrotransposon insertion in the domesticated loss-of-shattering allele SiLes1-TE (transposable element). This resource will enhance the utility of S. viridis for dissection of complex traits and biotechnological improvement of panicoid crops.
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http://dx.doi.org/10.1038/s41587-020-0681-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7536120PMC
October 2020

Cytokinin biosynthesis and transport for systemic nitrogen signaling.

Plant J 2021 01 27;105(2):421-430. Epub 2020 Oct 27.

Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601, Japan.

The plasticity of growth and development in response to environmental changes is one of the essential aspects of plant behavior. Cytokinins play an important role as signaling molecules in the long-distance communication between organs in systemic growth regulation in response to nitrogen. The spatial distribution of the expression sites of cytokinin biosynthesis genes leads to structural differences in the molecular species transported through the xylem and phloem, giving root-borne trans-hydroxylated cytokinins, namely trans-zeatin (tZ) type, a specialized efficacy in regulating shoot growth. Furthermore, root-to-shoot translocation via the xylem, tZ, and its precursor, the tZ riboside, controls different sets of shoot growth traits to fine-tune shoot growth in response to nitrogen availability. In addition to nitrogen, photosynthetically generated sugars positively regulate de novo cytokinin biosynthesis in the roots, and contribute to plant growth under elevated CO conditions. In shoot-to-root signaling, cytokinins also play a role in the regulation of nutrient acquisition and root system growth in cooperation with other types of signaling molecules, such as C-TERMINALLY ENCODED PEPTIDE DOWNSTREAMs. As cytokinin is a key regulator for the maintenance of shoot apical meristem, deepening our understanding of the regulatory mechanisms of cytokinin biosynthesis and transport in response to nitrogen is important not only for basic comprehension of plant growth, but also to ensure the stability of agricultural production.
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http://dx.doi.org/10.1111/tpj.15011DOI Listing
January 2021

Fruit setting rewires central metabolism via gibberellin cascades.

Proc Natl Acad Sci U S A 2020 09 3;117(38):23970-23981. Epub 2020 Sep 3.

Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan;

Fruit set is the process whereby ovaries develop into fruits after pollination and fertilization. The process is induced by the phytohormone gibberellin (GA) in tomatoes, as determined by the constitutive GA response mutant However, the role of GA on the metabolic behavior in fruit-setting ovaries remains largely unknown. This study explored the biochemical mechanisms of fruit set using a network analysis of integrated transcriptome, proteome, metabolome, and enzyme activity data. Our results revealed that fruit set involves the activation of central carbon metabolism, with increased hexoses, hexose phosphates, and downstream metabolites, including intermediates and derivatives of glycolysis, the tricarboxylic acid cycle, and associated organic and amino acids. The network analysis also identified the transcriptional hub gene , that coordinated metabolic activation. Furthermore, a kinetic model of sucrose metabolism predicted that the sucrose cycle had high activity levels in unpollinated ovaries, whereas it was shut down when sugars rapidly accumulated in vacuoles in fruit-setting ovaries, in a time-dependent manner via tonoplastic sugar carriers. Moreover, fruit set at least partly required the activity of fructokinase, which may pull fructose out of the vacuole, and this could feed the downstream pathways. Collectively, our results indicate that GA cascades enhance sink capacities, by up-regulating central metabolic enzyme capacities at both transcriptional and posttranscriptional levels. This leads to increased sucrose uptake and carbon fluxes for the production of the constituents of biomass and energy that are essential for rapid ovary growth during the initiation of fruit set.
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http://dx.doi.org/10.1073/pnas.2011859117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7519230PMC
September 2020

Integrative omics approaches revealed a crosstalk among phytohormones during tuberous root development in cassava.

Plant Mol Biol 2020 Aug 5. Epub 2020 Aug 5.

RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan.

Key Message: Integrative omics approaches revealed a crosstalk among phytohormones during tuberous root development in cassava. Tuberous root formation is a complex process consisting of phase changes as well as cell division and elongation for radial growth. We performed an integrated analysis to clarify the relationships among metabolites, phytohormones, and gene transcription during tuberous root formation in cassava (Manihot esculenta Crantz). We also confirmed the effects of the auxin (AUX), cytokinin (CK), abscisic acid (ABA), jasmonic acid (JA), gibberellin (GA), brassinosteroid (BR), salicylic acid, and indole-3-acetic acid conjugated with aspartic acid on tuberous root development. An integrated analysis of metabolites and gene expression indicated the expression levels of several genes encoding enzymes involved in starch biosynthesis and sucrose metabolism are up-regulated during tuberous root development, which is consistent with the accumulation of starch, sugar phosphates, and nucleotides. An integrated analysis of phytohormones and gene transcripts revealed a relationship among AUX signaling, CK signaling, and BR signaling, with AUX, CK, and BR inducing tuberous root development. In contrast, ABA and JA inhibited tuberous root development. These phenomena might represent the differences between stem tubers (e.g., potato) and root tubers (e.g., cassava). On the basis of these results, a phytohormonal regulatory model for tuberous root development was constructed. This model may be useful for future phytohormonal studies involving cassava.
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http://dx.doi.org/10.1007/s11103-020-01033-8DOI Listing
August 2020

The inhibition of SlIAA9 mimics an increase in endogenous auxin and mediates changes in auxin and gibberellin signalling during parthenocarpic fruit development in tomato.

J Plant Physiol 2020 Sep 16;252:153238. Epub 2020 Jul 16.

Faculty of Life and Environmental Sciences, University of Tsukuba, Tennodai 1-1-1 Tsukuba, Ibaraki 305-8572, Japan; Tsukuba Plant Innovation Research Center, University of Tsukuba, Tennodai 1-1-1, Tsukuba, Ibaraki, 305-8572, Japan. Electronic address:

Parthenocarpic fruit formation can be achieved through the inhibition of SlIAA9, a negative regulator of auxin signalling in tomato plant. During early fruit development under SlIAA9 inhibition, cell division and cell expansion were observed. Bioactive gibberellin (GA) accumulated, but indole-3-acetic acid (IAA) and trans-zeatin did not accumulate substantially. Furthermore, under SlIAA9 inhibition, auxin-responsive genes such as SlIAA2, -3, and -14 were upregulated, and SlARF7 was downregulated. These results indicate that SlIAA9 inhibition mimics an increase in auxin. The auxin biosynthesis genes SlTAR1, ToFZY, and ToFZY5 were stimulated by an increase in auxin and by auxin mimicking under SlIAA9 inhibition. However, SlTAR2 and ToFZY2 were upregulated only by pollination followed by high IAA accumulation. These results suggest that SlTAR2 and ToFZY2 play an important role in IAA synthesis in growing ovaries. GA synthesis was also activated by SlIAA9 inhibition through both the early-13-hydroxylation (for GA synthesis) and non-13-hydroxylation (GA) pathways, indicating that fruit set caused by SlIAA9 inhibition was partially mediated by the GA pathway. SlIAA9 inhibition induced the expression of GA inactivation genes as well as GA biosynthesis genes except SlCPS during early parthenocarpic fruit development in tomato. This result suggests that inactivation genes play a role in fine-tuning the regulation of bioactive GA accumulation.
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http://dx.doi.org/10.1016/j.jplph.2020.153238DOI Listing
September 2020

Antagonistic regulation of the gibberellic acid response during stem growth in rice.

Nature 2020 08 15;584(7819):109-114. Epub 2020 Jul 15.

Bioscience and Biotechnology Center, Nagoya University, Nagoya, Japan.

The size of plants is largely determined by growth of the stem. Stem elongation is stimulated by gibberellic acid. Here we show that internode stem elongation in rice is regulated antagonistically by an 'accelerator' and a 'decelerator' in concert with gibberellic acid. Expression of a gene we name ACCELERATOR OF INTERNODE ELONGATION 1 (ACE1), which encodes a protein of unknown function, confers cells of the intercalary meristematic region with the competence for cell division, leading to internode elongation in the presence of gibberellic acid. By contrast, upregulation of DECELERATOR OF INTERNODE ELONGATION 1 (DEC1), which encodes a zinc-finger transcription factor, suppresses internode elongation, whereas downregulation of DEC1 allows internode elongation. We also show that the mechanism of internode elongation that is mediated by ACE1 and DEC1 is conserved in the Gramineae family. Furthermore, an analysis of genetic diversity suggests that mutations in ACE1 and DEC1 have historically contributed to the selection of shorter plants in domesticated populations of rice to increase their resistance to lodging, and of taller plants in wild species of rice for adaptation to growth in deep water. Our identification of these antagonistic regulatory factors enhances our understanding of the gibberellic acid response as an additional mechanism that regulates internode elongation and environmental fitness, beyond biosynthesis and gibberellic acid signal transduction.
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http://dx.doi.org/10.1038/s41586-020-2501-8DOI Listing
August 2020

Diverse panicle architecture results from various combinations of Prl5/GA20ox4 and Pbl6/APO1 alleles.

Commun Biol 2020 06 11;3(1):302. Epub 2020 Jun 11.

Bioscience and Biotechnology Center, Nagoya University, Nagoya, Aichi, 464-8601, Japan.

Panicle architecture directly affects crop productivity and is a key target of high-yield rice breeding. Panicle length strongly affects panicle architecture, but the underlying regulatory mechanisms are largely unknown. Here, we show that two quantitative trait loci (QTLs), PANICLE RACHIS LENGTH5 (Prl5) and PRIMARY BRANCH LENGTH6 (Pbl6), independently regulate panicle length in rice. Prl5 encodes a gibberellin biosynthesis enzyme, OsGA20ox4. The expression of Prl5 was higher in young panicles resulting in panicle rachis elongation. Pbl6 is identical to ABERRANT PANICLE ORGANIZATION 1 (APO1), encoding an F-box-containing protein. We found a novel function that higher expression of Pbl6 is responsible for primary branch elongation. RNA-seq analysis revealed that these two genes independently regulate panicle length at the level of gene expression. QTL pyramiding of both genes increased panicle length and productivity. By combining these two genes in various combinations, we designed numerous panicle architecture without trade-off relationship.
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http://dx.doi.org/10.1038/s42003-020-1036-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7289860PMC
June 2020

Differences in xylem development between Dutch and Japanese tomato (Solanum lycopersicum) correlate with cytokinin levels in hypocotyls.

Ann Bot 2020 07;126(2):315-322

Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa, Nagoya, Japan.

Background And Aims: Dutch tomato cultivars tend to have a greater yield than Japanese cultivars even if they are grown under the same conditions. Factors contributing to the increased yield of the Dutch cultivars were a greater light use efficiency and greater leaf photosynthetic rate. On the other hand, the relationship between tomato yields and anatomical traits is still unclear. The aim of this study is to identify the anatomical traits related to the difference in yield between Dutch and Japanese cultivars.

Methods: Anatomical properties were compared during different growth stages of Dutch and Japanese tomatoes. Hormone profiles and related gene expression in hypocotyls of Dutch and Japanese cultivars were compared in the hypocotyls of 3- and 4-week-old plants.

Key Results: Dutch cultivars have a more developed secondary xylem than Japanese cultivars, which would allow for greater transport of water, mineral nutrients and phytohormones to the shoots. The areas and ratios of the xylem in the hypocotyls of 3- to 6-week-old plants were larger in the Dutch cultivars. In reciprocal grafts of the Japanese and Dutch cultivars, xylem development at the scion and rootstock depended on the scion cultivar, suggesting that some factors in the scion are responsible for the difference in xylem development. The cytokinin content, especially the level of N6-(Δ 2-isopentenyl) adenine (iP)-type cytokinin, was higher in the Dutch cultivars. This result was supported by the greater expression of Sl-IPT3 (a cytokinin biosynthesis gene) and Sl-RR16/17 (a cytokinin-responsive gene) in the Dutch cultivars.

Conclusions: These results suggest that iP-type cytokinins, which are locally synthesized in the hypocotyl, contribute to xylem development. The greater xylem development in Dutch cultivars might contribute to the high yield of the tomato.
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http://dx.doi.org/10.1093/aob/mcaa094DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7380485PMC
July 2020

Columnar growth phenotype in apple results from gibberellin deficiency by ectopic expression of a dioxygenase gene.

Tree Physiol 2020 08;40(9):1205-1216

Division of Apple Research, Institute of Fruit Tree and Tea Science, National Agriculture and Food Research Organization, 92-24 Nabeyashiki, Shimokuriyagawa, Morioka, Iwate 020-0123, Japan.

The apple cultivar McIntosh Wijcik, which is a mutant of 'McIntosh', exhibits a columnar growth phenotype (short internodes, few lateral branches, many spurs, etc.) that is controlled by a dominant Co gene. The candidate gene (MdDOX-Co), encoding a 2-oxoglutarate-dependent dioxygenase, is located adjacent to an insertion mutation. Non-columnar apples express MdDOX-Co in the roots, whereas columnar apples express MdDOX-Co in the aerial parts as well as in the roots. However, the function of MdDOX-Co remains unknown. Here, we characterized tobacco plants overexpressing MdDOX-Co. The tobacco plants showed the typical dwarf phenotype, which was restored by application of gibberellin A3 (GA3). Moreover, the dwarf tobacco plants had low concentrations of endogenous bioactive gibberellin A1 (GA1) and gibberellin A4 (GA4). Similarly, 'McIntosh Wijcik' contained low endogenous GA4 concentration and its dwarf traits (short main shoot and internodes) were partially reversed by GA3 application. These results indicate that MdDOX-Co is associated with bioactive GA deficiency. Interestingly, GA3 application to apple trees also resulted in an increased number of lateral branches and a decrease in flower bud number, indicating that gibberellin (GA) plays important roles in regulating apple tree architecture by affecting both lateral branch formation (vegetative growth) and flower bud formation (reproductive growth). We propose that a deficiency of bioactive GA by ectopic expression of MdDOX-Co in the aerial parts of columnar apples not only induces dwarf phenotypes but also inhibits lateral branch development and promotes flower bud formation, and assembly of these multiple phenotypes constructs the columnar tree form.
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http://dx.doi.org/10.1093/treephys/tpaa049DOI Listing
August 2020

Force-Generating Mechanism of Axonemal Dynein in Solo and Ensemble.

Int J Mol Sci 2020 Apr 18;21(8). Epub 2020 Apr 18.

Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, Osaka 5650871, Japan.

In eukaryotic cilia and flagella, various types of axonemal dyneins orchestrate their distinct functions to generate oscillatory bending of axonemes. The force-generating mechanism of dyneins has recently been well elucidated, mainly in cytoplasmic dyneins, thanks to progress in single-molecule measurements, X-ray crystallography, and advanced electron microscopy. These techniques have shed light on several important questions concerning what conformational changes accompany ATP hydrolysis and whether multiple motor domains are coordinated in the movements of dynein. However, due to the lack of a proper expression system for axonemal dyneins, no atomic coordinates of the entire motor domain of axonemal dynein have been reported. Therefore, a substantial amount of knowledge on the molecular architecture of axonemal dynein has been derived from electron microscopic observations on dynein arms in axonemes or on isolated axonemal dynein molecules. This review describes our current knowledge and perspectives of the force-generating mechanism of axonemal dyneins in solo and in ensemble.
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http://dx.doi.org/10.3390/ijms21082843DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7215579PMC
April 2020

The Maize () Mutation Alters Leaf Patterning through Increased Cytokinin Signaling.

Plant Cell 2020 05 23;32(5):1501-1518. Epub 2020 Mar 23.

Corteva Agriscience, Johnston, Iowa 50131.

Leaf morphogenesis requires growth polarized along three axes-proximal-distal (P-D) axis, medial-lateral axis, and abaxial-adaxial axis. Grass leaves display a prominent P-D polarity consisting of a proximal sheath separated from the distal blade by the auricle and ligule. Although proper specification of the four segments is essential for normal morphology, our knowledge is incomplete regarding the mechanisms that influence P-D specification in monocots such as maize (). Here, we report the identification of the gene underlying the semidominant, leaf patterning maize mutant (). plants produce leaves with outgrowths consisting of proximal segments-sheath, auricle, and ligule-emanating from the distal blade margin. Analysis of three independent alleles revealed gain-of-function missense mutations in the ligand binding domain of the maize cytokinin (CK) receptor () gene. Biochemical analysis and structural modeling suggest the mutated residues near the CK binding pocket affect CK binding affinity. Treatment of the wild-type seedlings with exogenous CK phenocopied the leaf phenotypes. Results from expression and epistatic analyses indicated the mutant receptor appears to be hypersignaling. Our results demonstrate that hypersignaling of CK in incipient leaf primordia can reprogram developmental patterns in maize.
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http://dx.doi.org/10.1105/tpc.19.00677DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7203929PMC
May 2020

Metabolite and Phytohormone Profiling Illustrates Metabolic Reprogramming as an Escape Strategy of Deepwater Rice during Partially Submerged Stress.

Metabolites 2020 Feb 14;10(2). Epub 2020 Feb 14.

RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa 230-0045, Japan.

Rice varieties that can survive under submergence conditions respond to flooding either by enhancing internode elongation or by quiescence of shoot elongation. Despite extensive efforts to identify key metabolites triggered by complete submergence of rice possessing UBMERGENCE () locus, metabolic responses of internode elongation of deepwater rice governed by the and genes remain elusive. This study investigated specific metabolomic responses under partial submergence (PS) to deepwater- (C9285) and non-deepwater rice cultivars (Taichung 65 (T65)). In addition, we examined the response in a near-isogenic line (NIL-12) that has a C9285 genomic fragment on chromosome 12 introgressed into the genetic background of T65. Under short-term submergence (0-24 h), metabolite profiles of C9285, NIL-12, and T65 were compared to extract significantly changed metabolites in deepwater rice under PS conditions. Comprehensive metabolite and phytohormone profiling revealed increases in metabolite levels in the glycolysis pathway in NIL-12 plants. Under long-term submergence (0-288 h), we found decreased amino acid levels. These metabolomic changes were opposite when compared to those in flood-tolerant rice with locus. Auxin conjugate levels related to stress response decreased in NIL-12 lines relative to T65. Our analysis helped clarify the complex metabolic reprogramming in deepwater rice as an escape strategy.
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http://dx.doi.org/10.3390/metabo10020068DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7074043PMC
February 2020

Metabolite/phytohormone-gene regulatory networks in soybean organs under dehydration conditions revealed by integration analysis.

Plant J 2020 07 3;103(1):197-211. Epub 2020 May 3.

RIKEN Center for Sustainable Resource Science, 3-1-1 Koyadai, Tsukuba, Ibaraki, 305-0074, Japan.

Metabolites, phytohormones, and genes involved in dehydration responses/tolerance have been predicted in several plants. However, metabolite/phytohormone-gene regulatory networks in soybean organs under dehydration conditions remain unclear. Here, we analyzed the organ specificity of metabolites, phytohormones, and gene transcripts and revealed the characteristics of their regulatory networks in dehydration-treated soybeans. Our metabolite/phytohormone analysis revealed the accumulation of raffinose, trehalose, and cis-zeatin (cZ) specifically in dehydration-treated roots. In dehydration-treated soybeans, raffinose, and trehalose might have additional roles not directly involved in protecting the photosynthetic apparatus; cZ might contribute to root elongation for water uptake from the moisture region in soil. Our integration analysis of metabolites-genes indicated that galactinol, raffinose, and trehalose levels were correlated with transcript levels for key enzymes (galactinol synthase, raffinose synthase, trehalose 6-phosphate synthase, trehalose 6-phosphate phosphatase) at the level of individual plants but not at the organ level under dehydration. Genes encoding these key enzymes were expressed in mainly the aerial parts of dehydration-treated soybeans. These results suggested that raffinose and trehalose are transported from aerial plant parts to the roots in dehydration-treated soybeans. Our integration analysis of phytohormones-genes indicated that cZ and abscisic acid (ABA) levels were correlated with transcript levels for key enzymes (cytokinin nucleoside 5'-monophosphate phosphoribohydrolase, cytokinin oxidases/dehydrogenases, 9-cis-epoxycarotenoid dioxygenase) at the level of individual plants but not at the organ level under dehydration conditions. Therefore, processes such as ABA and cZ transport, among others, are important for the organ specificity of ABA and cZ production under dehydration conditions.
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http://dx.doi.org/10.1111/tpj.14719DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7384127PMC
July 2020

Overexpression of Sucrose Phosphate Synthase Enhanced Sucrose Content and Biomass Production in Transgenic Sugarcane.

Plants (Basel) 2020 Feb 6;9(2). Epub 2020 Feb 6.

Center for Development of Advanced Science and Technology (CDAST), University of Jember, Jember 68121, Indonesia.

Sucrose phosphate synthase (SPS) is a key enzyme in sucrose synthesis, which controls sucrose content in plants. This study was designed to examine the efficacy of the overexpression of gene on sucrose accumulation and carbon partitioning in transgenic sugarcane. The overexpression of gene increased SPS activity and sucrose content in transgenic sugarcane leaves. More importantly, the overexpression enhanced soluble acid invertase (SAI) activity concomitant with the increase of glucose and fructose levels in the leaves, whereas sucrose synthase activity exhibited almost no change. In the stalk, a similar correlation was observed, but a higher correlation was noted between SPS activity and sugar content. These results suggest that SPS overexpression has both direct and indirect effects on sugar concentration and SAI activity in sugarcane. In addition, SPS overexpression resulted in a significant increase in plant height and stalk number in some transgenic lines compared to those in non-transgenic control. Taken together, these results strongly suggest that enhancing SPS activity is a useful strategy for improving sugarcane yield.
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http://dx.doi.org/10.3390/plants9020200DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7076389PMC
February 2020

Flowering time control in rice by introducing Arabidopsis clock-associated PSEUDO-RESPONSE REGULATOR 5.

Biosci Biotechnol Biochem 2020 May 27;84(5):970-979. Epub 2020 Jan 27.

RIKEN Center for Sustainable Resource Science, Yokohama, Japan.

Plants flower under appropriate day-length conditions by integrating temporal information provided by the circadian clock with light and dark information from the environment. A sub-group of plant specific circadian clock-associated () genes (PRR7/PRR3 sub-group) controls flowering time both in long-day and short-day plants; however, flowering control by the other two PRR gene sub-groups has been reported only in (Arabidopsis), a model long-day plant. Here, we show that an Arabidopsis PRR9/PRR5 sub-group gene can control flowering time (heading date) in rice, a short-day plant. Although PRR5 promotes flowering in Arabidopsis, transgenic rice overexpressing Arabidopsis PRR5 caused late flowering. Such transgenic rice plants produced significantly higher biomass, but not grain yield, due to the late flowering. Concomitantly, expression of , a rice florigen gene, was reduced in the transgenic rice. CCT: CONSTANS, CONSTANS-LIKE, and TOC1; HD: HEADING DATE; LHY: LATE ELONGATED HYPOCOTYL; ; PR: pseudo-receiver; PRR: PSEUDO-RESPONSE REGULATOR; TOC1: TIMING OF CAB EXPRESSION 1; ZTL: ZEITLUPE.
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http://dx.doi.org/10.1080/09168451.2020.1719822DOI Listing
May 2020

Harnessing symbiotic plant-fungus interactions to unleash hidden forces from extreme plant ecosystems.

J Exp Bot 2020 06;71(13):3865-3877

Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentación (INIA), Campus de Montegancedo, Pozuelo de Alarcón (Madrid), Spain.

Global climate change is arguably one of the biggest threats of modern times and has already led to a wide range of impacts on the environment, economy, and society. Owing to past emissions and climate system inertia, global climate change is predicted to continue for decades even if anthropogenic greenhouse gas emissions were to stop immediately. In many regions, such as central Europe and the Mediterranean region, the temperature is likely to rise by 2-5 °C and annual precipitation is predicted to decrease. Expected heat and drought periods followed by floods, and unpredictable growing seasons, are predicted to have detrimental effects on agricultural production systems, causing immense economic losses and food supply problems. To mitigate the risks of climate change, agricultural innovations counteracting these effects need to be embraced and accelerated. To achieve maximum improvement, the required agricultural innovations should not focus only on crops but rather pursue a holistic approach including the entire ecosystem. Over millions of years, plants have evolved in close association with other organisms, particularly soil microbes that have shaped their evolution and contemporary ecology. Many studies have already highlighted beneficial interactions among plants and the communities of microorganisms with which they coexist. Questions arising from these discoveries are whether it will be possible to decipher a common molecular pattern and the underlying biochemical framework of interspecies communication, and whether such knowledge can be used to improve agricultural performance under environmental stress conditions. In this review, we summarize the current knowledge of plant interactions with fungal endosymbionts found in extreme ecosystems. Special attention will be paid to the interaction of plants with the symbiotic root-colonizing endophytic fungus Serendipita indica, which has been developed as a model system for beneficial plant-fungus interactions.
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http://dx.doi.org/10.1093/jxb/eraa040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7316966PMC
June 2020

Molecular Basis for Natural Vegetative Propagation via Regeneration in North American Lake Cress, Rorippa aquatica (Brassicaceae).

Plant Cell Physiol 2020 Feb;61(2):353-369

Faculty of Life Sciences, Kyoto Sangyo University, Kamigamo-Motoyama, Kita-Ku, Kyoto, 603-8555 Japan.

Some plant species have a striking capacity for regeneration in nature, including regeneration of the entire individual from explants. However, due to the lack of suitable experimental models, the regulatory mechanisms of spontaneous whole plant regeneration are mostly unknown. In this study, we established a novel model system to study these mechanisms using an amphibious plant within Brassicaceae, Rorippa aquatica, which naturally undergoes vegetative propagation via regeneration from leaf fragments. Morphological and anatomical observation showed that both de novo root and shoot organogenesis occurred from the proximal side of the cut edge transversely with leaf vascular tissue. Time-series RNA-seq analysis revealed that auxin and cytokinin responses were activated after leaf amputation and that regeneration-related genes were upregulated mainly on the proximal side of the leaf explants. Accordingly, we found that both auxin and cytokinin accumulated on the proximal side. Application of a polar auxin transport inhibitor retarded root and shoot regeneration, suggesting that the enhancement of auxin responses caused by polar auxin transport enhanced de novo organogenesis at the proximal wound site. Exogenous phytohormone and inhibitor applications further demonstrated that, in R. aquatica, both auxin and gibberellin are required for root regeneration, whereas cytokinin is important for shoot regeneration. Our results provide a molecular basis for vegetative propagation via de novo organogenesis.
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http://dx.doi.org/10.1093/pcp/pcz202DOI Listing
February 2020

Genome Sequence of Striga asiatica Provides Insight into the Evolution of Plant Parasitism.

Curr Biol 2019 09 12;29(18):3041-3052.e4. Epub 2019 Sep 12.

Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi 980-8577, Japan; Department of Agricultural Chemistry, School of Agriculture, Meiji University, Kawasaki, Kanagawa 214-8571, Japan.

Parasitic plants in the genus Striga, commonly known as witchweeds, cause major crop losses in sub-Saharan Africa and pose a threat to agriculture worldwide. An understanding of Striga parasite biology, which could lead to agricultural solutions, has been hampered by the lack of genome information. Here, we report the draft genome sequence of Striga asiatica with 34,577 predicted protein-coding genes, which reflects gene family contractions and expansions that are consistent with a three-phase model of parasitic plant genome evolution. Striga seeds germinate in response to host-derived strigolactones (SLs) and then develop a specialized penetration structure, the haustorium, to invade the host root. A family of SL receptors has undergone a striking expansion, suggesting a molecular basis for the evolution of broad host range among Striga spp. We found that genes involved in lateral root development in non-parasitic model species are coordinately induced during haustorium development in Striga, suggesting a pathway that was partly co-opted during the evolution of the haustorium. In addition, we found evidence for horizontal transfer of host genes as well as retrotransposons, indicating gene flow to S. asiatica from hosts. Our results provide valuable insights into the evolution of parasitism and a key resource for the future development of Striga control strategies.
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http://dx.doi.org/10.1016/j.cub.2019.07.086DOI Listing
September 2019

A Positive Feedback Loop Comprising LHW-TMO5 and Local Auxin Biosynthesis Regulates Initial Vascular Development in Arabidopsis Roots.

Plant Cell Physiol 2019 Dec;60(12):2684-2691

Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033 Japan.

The phytohormone auxin governs various developmental processes in plants including vascular formation. Auxin transport and biosynthesis are important factors in determining auxin distribution in tissues. Although the role of auxin transport in vein pattern formation is widely recognized, that of auxin biosynthesis in vascular development is poorly understood. Heterodimer complexes comprising two basic helix-loop-helix protein families, LONESOME HIGHWAY (LHW) and TARGET OF MONOPTEROS5 (TMO5)/TMO5-LIKE1 (T5L1), are master transcriptional regulators of the initial process of vascular development. The LHW-TMO5/T5L1 dimers regulate vascular initial cell production, vascular cell proliferation and xylem fate determination in the embryo and root apical meristem (RAM). In this study, we investigated the function of local auxin biosynthesis in initial vascular development in RAM. Results showed that LHW-T5L1 upregulated the expression of YUCCA4 (YUC4), a key auxin biosynthesis gene. The expression of YUC4 was essential for promoting xylem differentiation and vascular cell proliferation in RAM. Conversely, auxin biosynthesis was required for maintaining the expression levels of LHW, TMO5/T5L1 and their targets. Our results suggest that local auxin biosynthesis forms a positive feedback loop for fine-tuning the level of LHW-TMO5/T5L1, which is necessary for initiating vascular development.
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http://dx.doi.org/10.1093/pcp/pcz156DOI Listing
December 2019
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