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1.
Development ; 151(20)2024 Oct 15.
Article in English | MEDLINE | ID: mdl-39133134

ABSTRACT

Rho/Rac of plant (ROP) GTPases are plant-specific proteins that function as molecular switches, activated by guanine nucleotide exchange factors (GEFs) and inactivated by GTPase-activating proteins (GAPs). The bryophyte Marchantia polymorpha contains single copies of ROP (MpROP), GEFs [ROPGEF and SPIKE (SPK)] and GAPs [ROPGAP and ROP ENHANCER (REN)]. MpROP regulates the development of various tissues and organs, such as rhizoids, gemmae and air chambers. The ROPGEF KARAPPO (MpKAR) is essential for gemma initiation, but the functions of other ROP regulatory factors are less understood. This study focused on two GAPs: MpROPGAP and MpREN. Mpren single mutants showed defects in thallus growth, rhizoid tip growth, gemma development, and air-chamber formation, whereas Mpropgap mutants showed no visible abnormalities. However, Mpropgap Mpren double mutants had more severe phenotypes than the Mpren single mutants, suggesting backup roles of MpROPGAP in processes involving MpREN. Overexpression of MpROPGAP and MpREN resulted in similar gametophyte defects, highlighting the importance of MpROP activation/inactivation cycling (or balancing). Thus, MpREN predominantly, and MpROPGAP as a backup, regulate gametophyte development, likely by controlling MpROP activation in M. polymorpha.


Subject(s)
Marchantia , Plant Proteins , Marchantia/genetics , Marchantia/metabolism , Marchantia/growth & development , Plant Proteins/metabolism , Plant Proteins/genetics , Gene Expression Regulation, Plant , Mutation/genetics , Guanine Nucleotide Exchange Factors/metabolism , Guanine Nucleotide Exchange Factors/genetics , GTPase-Activating Proteins/metabolism , GTPase-Activating Proteins/genetics , Organogenesis, Plant/genetics , rho GTP-Binding Proteins/metabolism , rho GTP-Binding Proteins/genetics
2.
Plant Cell ; 36(6): 2359-2374, 2024 May 29.
Article in English | MEDLINE | ID: mdl-38445764

ABSTRACT

Plants have an astonishing ability to regenerate new organs after wounding. Here, we report that the wound-inducible transcription factor ENHANCER OF SHOOT REGENERATION1 (ESR1) has a dual mode of action in activating ANTHRANILATE SYNTHASE ALPHA SUBUNIT1 (ASA1) expression to ensure auxin-dependent de novo root organogenesis locally at wound sites of Arabidopsis (Arabidopsis thaliana) leaf explants. In the first mode, ESR1 interacts with HISTONE DEACETYLASE6 (HDA6), and the ESR1-HDA6 complex directly binds to the JASMONATE-ZIM DOMAIN5 (JAZ5) locus, inhibiting JAZ5 expression through histone H3 deacetylation. As JAZ5 interferes with the action of ETHYLENE RESPONSE FACTOR109 (ERF109), the transcriptional repression of JAZ5 at the wound site allows ERF109 to activate ASA1 expression. In the second mode, the ESR1 transcriptional activator directly binds to the ASA1 promoter to enhance its expression. Overall, our findings indicate that the dual biochemical function of ESR1, which specifically occurs near wound sites of leaf explants, maximizes local auxin biosynthesis and de novo root organogenesis in Arabidopsis.


Subject(s)
Arabidopsis Proteins , Arabidopsis , Gene Expression Regulation, Plant , Organogenesis, Plant , Plant Roots , Transcription Factors , Arabidopsis/genetics , Arabidopsis/growth & development , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Histone Deacetylases/metabolism , Histone Deacetylases/genetics , Indoleacetic Acids/metabolism , Organogenesis, Plant/genetics , Plant Leaves/genetics , Plant Leaves/metabolism , Plant Leaves/growth & development , Plant Roots/growth & development , Plant Roots/genetics , Plants, Genetically Modified , Promoter Regions, Genetic/genetics , Transcription Factors/metabolism , Transcription Factors/genetics
3.
Plant Cell ; 34(11): 4554-4568, 2022 10 27.
Article in English | MEDLINE | ID: mdl-35972347

ABSTRACT

Wounded plant cells can form callus to seal the wound site. Alternatively, wounding can cause adventitious organogenesis or somatic embryogenesis. These distinct developmental pathways require specific cell fate decisions. Here, we identify GhTCE1, a basic helix-loop-helix family transcription factor, and its interacting partners as a central regulatory module of early cell fate transition during in vitro dedifferentiation of cotton (Gossypium hirsutum). RNAi- or CRISPR/Cas9-mediated loss of GhTCE1 function resulted in excessive accumulation of reactive oxygen species (ROS), arrested callus cell elongation, and increased adventitious organogenesis. In contrast, GhTCE1-overexpressing tissues underwent callus cell growth, but organogenesis was repressed. Transcriptome analysis revealed that several pathways depend on proper regulation of GhTCE1 expression, including lipid transfer pathway components, ROS homeostasis, and cell expansion. GhTCE1 bound to the promoters of the target genes GhLTP2 and GhLTP3, activating their expression synergistically, and the heterodimer TCE1-TCEE1 enhances this activity. GhLTP2- and GhLTP3-deficient tissues accumulated ROS and had arrested callus cell elongation, which was restored by ROS scavengers. These results reveal a unique regulatory network involving ROS and lipid transfer proteins, which act as potential ROS scavengers. This network acts as a switch between unorganized callus growth and organized development during in vitro dedifferentiation of cotton cells.


Subject(s)
Basic Helix-Loop-Helix Transcription Factors , Cellular Reprogramming , Gene Expression Regulation, Plant , Gossypium , Organogenesis, Plant , Plant Proteins , Gene Expression Profiling , Gene Expression Regulation, Plant/genetics , Gossypium/genetics , Gossypium/growth & development , Plant Proteins/genetics , Plant Proteins/metabolism , Reactive Oxygen Species/metabolism , Lipid Metabolism/genetics , Basic Helix-Loop-Helix Transcription Factors/genetics , Basic Helix-Loop-Helix Transcription Factors/metabolism , Enhancer Elements, Genetic , Protein Multimerization , Cellular Reprogramming/genetics , Organogenesis, Plant/genetics
4.
Plant Cell ; 34(1): 228-246, 2022 01 20.
Article in English | MEDLINE | ID: mdl-34459922

ABSTRACT

Bryophytes are nonvascular spore-forming plants. Unlike in flowering plants, the gametophyte (haploid) generation of bryophytes dominates the sporophyte (diploid) generation. A comparison of bryophytes with flowering plants allows us to answer some fundamental questions raised in evolutionary cell and developmental biology. The moss Physcomitrium patens was the first bryophyte with a sequenced genome. Many cell and developmental studies have been conducted in this species using gene targeting by homologous recombination. The liverwort Marchantia polymorpha has recently emerged as an excellent model system with low genomic redundancy in most of its regulatory pathways. With the development of molecular genetic tools such as efficient genome editing, both P. patens and M. polymorpha have provided many valuable insights. Here, we review these advances with a special focus on polarity formation at the cell and tissue levels. We examine current knowledge regarding the cellular mechanisms of polarized cell elongation and cell division, including symmetric and asymmetric cell division. We also examine the role of polar auxin transport in mosses and liverworts. Finally, we discuss the future of evolutionary cell and developmental biological studies in plants.


Subject(s)
Biological Evolution , Bryopsida/physiology , Cell Polarity , Indoleacetic Acids/metabolism , Marchantia/physiology , Plant Cells/physiology , Biological Transport , Bryopsida/growth & development , Cell Biology , Cell Division , Cell Enlargement , Developmental Biology , Marchantia/growth & development , Organogenesis, Plant , Plant Growth Regulators/metabolism
5.
Proc Natl Acad Sci U S A ; 119(50): e2215569119, 2022 12 13.
Article in English | MEDLINE | ID: mdl-36469773

ABSTRACT

The flattened leaf form is an important adaptation for efficient photosynthesis, and the developmental process of flattened leaves has been intensively studied. Classic microsurgery studies in potato and tomato suggest that the shoot apical meristem (SAM) communicates with the leaf primordia to promote leaf blade formation. More recently, it was found that polar auxin transport (PAT) could mediate this communication. However, it is unclear how the expression of leaf patterning genes is tailored by PAT routes originating from SAM. By combining experimental observations and computer model simulations, we show that microsurgical incisions and local inhibition of PAT in tomato interfere with auxin transport toward the leaf margins, reducing auxin response levels and altering the leaf blade shape. Importantly, oval auxin responses result in the bipolar expression of SlLAM1 that determines leaf blade formation. Furthermore, wounding caused by incisions promotes degradation of SlREV, a known regulator of leaf polarity. Additionally, computer simulations suggest that local auxin biosynthesis in early leaf primordia could remove necessity for external auxin supply originating from SAM, potentially explaining differences between species. Together, our findings establish how PAT near emerging leaf primordia determines spatial auxin patterning and refines SlLAM1 expression in the leaf margins to guide leaf flattening.


Subject(s)
Indoleacetic Acids , Solanum lycopersicum , Indoleacetic Acids/metabolism , Meristem/metabolism , Plant Leaves/metabolism , Biological Transport/genetics , Organogenesis, Plant , Solanum lycopersicum/genetics , Solanum lycopersicum/metabolism , Gene Expression Regulation, Plant
6.
Proc Natl Acad Sci U S A ; 119(27): e2202669119, 2022 07 05.
Article in English | MEDLINE | ID: mdl-35763576

ABSTRACT

Induction of a pluripotent cell mass, called callus, from detached organs is an initial step in in vitro plant regeneration, during which phytohormone auxin-induced ectopic activation of a root developmental program has been shown to be required for subsequent de novo regeneration of shoots and roots. However, whether other signals are involved in governing callus formation, and thus plant regeneration capability, remains largely unclear. Here, we report that the Arabidopsis calcium (Ca2+) signaling module CALMODULIN IQ-MOTIF CONTAINING PROTEIN (CaM-IQM) interacts with auxin signaling to regulate callus and lateral root formation. We show that disruption of IQMs or CaMs retards auxin-induced callus and lateral root formation by dampening auxin responsiveness, and that CaM-IQM complexes physically interact with the auxin signaling repressors INDOLE-3-ACETIC ACID INDUCIBLE (IAA) proteins in a Ca2+-dependent manner. We further provide evidence that the physical interaction of CaM6 with IAA19 destabilizes the repressive interaction of IAA19 with AUXIN RESPONSE FACTOR 7 (ARF7), and thus regulates auxin-induced callus formation. These findings not only define a critical role of CaM-IQM-mediated Ca2+ signaling in callus and lateral root formation, but also provide insight into the interplay of Ca2+ signaling and auxin actions during plant regeneration and development.


Subject(s)
Arabidopsis Proteins , Arabidopsis , Calcium Signaling , Organogenesis, Plant , Plant Roots , Arabidopsis/growth & development , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Calmodulin/metabolism , Indoleacetic Acids/metabolism , Plant Roots/growth & development , Plant Roots/metabolism , Transcription Factors/metabolism
7.
EMBO J ; 39(2): e101928, 2020 01 15.
Article in English | MEDLINE | ID: mdl-31777974

ABSTRACT

The UV-B photoreceptor UVR8 mediates multiple UV-B responses in plants, but the function of UVR8 in regulating root development has not previously been investigated. Here, we show that UV-B light inhibits Arabidopsis lateral root growth in a UVR8-dependent manner. Monomeric UVR8 inhibits auxin responses in a tissue-autonomous manner and thereby regulates lateral root growth. Genome-wide gene expression analysis demonstrated that auxin and UV-B irradiation antagonistically regulate auxin-regulated gene expression. We further show that UVR8 physically interacts with MYB73/MYB77 (MYB DOMAIN PROTEIN 73/77) in a UV-B-dependent manner. UVR8 inhibits lateral root development via regulation of MYB73/MYB77. When activated by UV-B light, UVR8 localizes to the nucleus and inhibits the DNA-binding activities of MYB73/MYB77 and directly represses the transcription of their target auxin-responsive genes. Our results demonstrate that UV-B light and UVR8 are critical for both shoot morphogenesis and root development. The UV-B-dependent interaction of UVR8 and MYB73/MYB77 serves as an important module that integrates light and auxin signaling and represents a new UVR8 signaling mechanism in plants.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/growth & development , Chromosomal Proteins, Non-Histone/metabolism , Indoleacetic Acids/pharmacology , Organogenesis, Plant/drug effects , Plant Roots/growth & development , Transcription Factors/metabolism , Arabidopsis/drug effects , Arabidopsis/metabolism , Arabidopsis/radiation effects , Arabidopsis Proteins/genetics , Chromosomal Proteins, Non-Histone/genetics , Plant Growth Regulators/pharmacology , Plant Roots/drug effects , Plant Roots/metabolism , Plant Roots/radiation effects , Signal Transduction , Transcription Factors/genetics , Ultraviolet Rays
8.
Development ; 148(6)2021 03 24.
Article in English | MEDLINE | ID: mdl-33762427

ABSTRACT

Plants encompass unparalleled multi-scale regenerative potential. Despite lacking specialized cells that are recruited to injured sites, and despite their cells being encased in rigid cell walls, plants exhibit a variety of regenerative responses ranging from the regeneration of specific cell types, tissues and organs, to the rebuilding of an entire organism. Over the years, extensive studies on embryo, shoot and root development in the model plant species Arabidopsis thaliana have provided insights into the mechanisms underlying plant regeneration. These studies highlight how Arabidopsis, with its wide array of refined molecular, genetic and cell biological tools, provides a perfect model to interrogate the cellular and molecular mechanisms of reprogramming during regeneration.


Subject(s)
Arabidopsis/metabolism , Arabidopsis/growth & development , Arabidopsis Proteins/metabolism , Gene Expression Regulation, Plant , Homeodomain Proteins/metabolism , Indoleacetic Acids/metabolism , Organogenesis, Plant/physiology , Plant Roots/growth & development , Plant Roots/metabolism , Plant Shoots/growth & development , Plant Shoots/metabolism , Stress, Mechanical
9.
New Phytol ; 244(3): 1057-1073, 2024 Nov.
Article in English | MEDLINE | ID: mdl-39140996

ABSTRACT

Bamboo with its remarkable growth rate and economic significance, offers an ideal system to investigate the molecular basis of organogenesis in rapidly growing plants, particular in monocots, where gene regulatory networks governing the maintenance and differentiation of shoot apical and intercalary meristems remain a subject of controversy. We employed both spatial and single-nucleus transcriptome sequencing on 10× platform to precisely dissect the gene functions in various tissues and early developmental stages of bamboo shoots. Our comprehensive analysis reveals distinct cell trajectories during shoot development, uncovering critical genes and pathways involved in procambium differentiation, intercalary meristem formation, and vascular tissue development. Spatial and temporal expression patterns of key regulatory genes, particularly those related to hormone signaling and lipid metabolism, strongly support the hypothesis that intercalary meristem origin from surrounded parenchyma cells. Specific gene expressions in intercalary meristem exhibit regular and dispersed distribution pattern, offering clues for understanding the intricate molecular mechanisms that drive the rapid growth of bamboo shoots. The single-nucleus and spatial transcriptome analysis reveal a comprehensive landscape of gene activity, enhancing the understanding of the molecular architecture of organogenesis and providing valuable resources for future genomic and genetic studies relying on identities of specific cell types.


Subject(s)
Gene Expression Regulation, Plant , Meristem , Plant Shoots , Transcriptome , Plant Shoots/growth & development , Plant Shoots/genetics , Transcriptome/genetics , Meristem/genetics , Meristem/growth & development , Organogenesis, Plant/genetics , Gene Expression Profiling , Spatio-Temporal Analysis , Sasa/genetics , Sasa/growth & development , Genes, Plant , Organogenesis/genetics , Time Factors , Cell Nucleus/metabolism , Cell Nucleus/genetics
10.
Proc Natl Acad Sci U S A ; 118(13)2021 03 30.
Article in English | MEDLINE | ID: mdl-33771923

ABSTRACT

Phyllotaxis, the distribution of organs such as leaves and flowers on their support, is a key attribute of plant architecture. The geometric regularity of phyllotaxis has attracted multidisciplinary interest for centuries, resulting in an understanding of the patterns in the model plants Arabidopsis and tomato down to the molecular level. Nevertheless, the iconic example of phyllotaxis, the arrangement of individual florets into spirals in the heads of the daisy family of plants (Asteraceae), has not been fully explained. We integrate experimental data and computational models to explain phyllotaxis in Gerbera hybrida We show that phyllotactic patterning in gerbera is governed by changes in the size of the morphogenetically active zone coordinated with the growth of the head. The dynamics of these changes divides the patterning process into three phases: the development of an approximately circular pattern with a Fibonacci number of primordia near the head rim, its gradual transition to a zigzag pattern, and the development of a spiral pattern that fills the head on the template of this zigzag pattern. Fibonacci spiral numbers arise due to the intercalary insertion and lateral displacement of incipient primordia in the first phase. Our results demonstrate the essential role of the growth and active zone dynamics in the patterning of flower heads.


Subject(s)
Asteraceae/physiology , Inflorescence/growth & development , Organogenesis, Plant , Asteraceae/anatomy & histology , Genes, Reporter , Indoleacetic Acids/metabolism , Inflorescence/anatomy & histology , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically Modified
11.
Int J Mol Sci ; 25(17)2024 Sep 03.
Article in English | MEDLINE | ID: mdl-39273513

ABSTRACT

The lateral root (LR) is an essential component of the plant root system, performing important functions for nutrient and water uptake in plants and playing a pivotal role in cereal crop productivity. Nitrate (NO3-) is an essential nutrient for plants. In this study, wheat plants were grown in 1/2 strength Hoagland's solution containing 5 mM NO3- (check; CK), 0.1 mM NO3- (low NO3-; LN), or 0.1 mM NO3- plus 60 mg/L 2,3,5-triiodobenzoic acid (TIBA) (LNT). The results showed that LN increased the LR number significantly at 48 h after treatment compared with CK, while not increasing the root biomass, and LNT significantly decreased the LR number and root biomass. The transcriptomic analysis showed that LN induced the expression of genes related to root IAA synthesis and transport and cell wall remodeling, and it was suppressed in the LNT conditions. A physiological assay revealed that the LN conditions increased the activity of IAA biosynthesis-related enzymes, the concentrations of tryptophan and IAA, and the activity of cell wall remodeling enzymes in the roots, whereas the content of polysaccharides in the LRP cell wall was significantly decreased compared with the control. Fourier-transform infrared spectroscopy and atomic microscopy revealed that the content of cell wall polysaccharides decreased and the cell wall elasticity of LR primordia (LRP) increased under the LN conditions. The effects of LN on IAA synthesis and polar transport, cell wall remodeling, and LR development were abolished when TIBA was applied. Our findings indicate that NO3- starvation may improve auxin homeostasis and the biological properties of the LRP cell wall and thus promote LR initiation, while TIBA addition dampens the effects of LN on auxin signaling, gene expression, physiological processes, and the root architecture.


Subject(s)
Gene Expression Regulation, Plant , Indoleacetic Acids , Nitrates , Plant Roots , Signal Transduction , Triticum , Triticum/metabolism , Triticum/genetics , Triticum/growth & development , Indoleacetic Acids/metabolism , Plant Roots/growth & development , Plant Roots/metabolism , Plant Roots/genetics , Plant Roots/drug effects , Nitrates/metabolism , Gene Expression Regulation, Plant/drug effects , Cell Wall/metabolism , Plant Proteins/metabolism , Plant Proteins/genetics , Organogenesis, Plant/genetics , Gene Expression Profiling
12.
Development ; 147(24)2020 12 15.
Article in English | MEDLINE | ID: mdl-33144393

ABSTRACT

Temperature is one of the most impactful environmental factors to which plants adjust their growth and development. Although the regulation of temperature signaling has been extensively investigated for the aerial part of plants, much less is known and understood about how roots sense and modulate their growth in response to fluctuating temperatures. Here, we found that shoot and root growth responses to high ambient temperature are coordinated during early seedling development in Arabidopsis A shoot signaling module that includes HY5, the phytochromes and the PIFs exerts a central function in coupling these growth responses and maintaining auxin levels in the root. In addition to the HY5/PIF-dependent shoot module, a regulatory axis composed of auxin biosynthesis and auxin perception factors controls root responses to high ambient temperature. Taken together, our findings show that shoot and root developmental responses to temperature are tightly coupled during thermomorphogenesis and suggest that roots integrate energy signals with local hormonal inputs.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/genetics , Basic-Leucine Zipper Transcription Factors/genetics , Morphogenesis/genetics , Organogenesis, Plant/genetics , Arabidopsis/growth & development , Gene Expression Regulation, Plant/genetics , Indoleacetic Acids/metabolism , Phytochrome/genetics , Plant Shoots/genetics , Plant Shoots/growth & development , Signal Transduction
13.
Development ; 147(14)2020 07 24.
Article in English | MEDLINE | ID: mdl-32611605

ABSTRACT

mRNA methylation at the N6-position of adenosine (m6A) enables multiple layers of post-transcriptional gene control, often via RNA-binding proteins that use a YT521-B homology (YTH) domain for specific m6A recognition. In Arabidopsis, normal leaf morphogenesis and rate of leaf formation require m6A and the YTH-domain proteins ECT2, ECT3 and ECT4. In this study, we show that ect2/ect3 and ect2/ect3/ect4 mutants also exhibit slow root and stem growth, slow flower formation, defective directionality of root growth, and aberrant flower and fruit morphology. In all cases, the m6A-binding site of ECT proteins is required for in vivo function. We also demonstrate that both m6A methyltransferase mutants and ect2/ect3/ect4 exhibit aberrant floral phyllotaxis. Consistent with the delayed organogenesis phenotypes, we observe particularly high expression of ECT2, ECT3 and ECT4 in rapidly dividing cells of organ primordia. Accordingly, ect2/ect3/ect4 mutants exhibit decreased rates of cell division in leaf and vascular primordia. Thus, the m6A-ECT2/ECT3/ECT4 axis is employed as a recurrent module to stimulate plant organogenesis, at least in part by enabling rapid cellular proliferation.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Intracellular Signaling Peptides and Proteins/metabolism , Organogenesis, Plant/genetics , Adenosine/metabolism , Arabidopsis/growth & development , Arabidopsis Proteins/antagonists & inhibitors , Arabidopsis Proteins/genetics , Binding Sites , Cell Proliferation , Flowers/growth & development , Flowers/metabolism , Gene Expression Regulation, Plant , Intracellular Signaling Peptides and Proteins/genetics , Methylation , Methyltransferases/genetics , Methyltransferases/metabolism , Mutagenesis, Site-Directed , Plant Leaves/cytology , Plant Leaves/growth & development , Plant Leaves/metabolism , Plant Roots/growth & development , Plant Roots/metabolism , Plant Stems/growth & development , Plant Stems/metabolism , Plants, Genetically Modified/growth & development , Plants, Genetically Modified/metabolism , Protein Binding , RNA Interference , RNA, Small Interfering/metabolism , RNA-Binding Proteins/antagonists & inhibitors , RNA-Binding Proteins/genetics , RNA-Binding Proteins/metabolism
14.
Plant Physiol ; 190(1): 500-515, 2022 08 29.
Article in English | MEDLINE | ID: mdl-35758633

ABSTRACT

Leaf angle is an important agronomic trait determining maize (Zea mays) planting density and light penetration into the canopy and contributes to the yield gain in modern maize hybrids. However, little is known about the molecular mechanisms underlying leaf angle beyond the ZmLG1 (liguleless1) and ZmLG2 (Liguleless2) genes. In this study, we found that the transcription factor (TF) ZmBEH1 (BZR1/BES1 homolog gene 1) is targeted by ZmLG2 and regulates leaf angle formation by influencing sclerenchyma cell layers on the adaxial side. ZmBEH1 interacted with the TF ZmBZR1 (Brassinazole Resistant 1), whose gene expression was also directly activated by ZmLG2. Both ZmBEH1 and ZmBZR1 are bound to the promoter of ZmSCL28 (SCARECROW-LIKE 28), a third TF that influences leaf angle. Our study demonstrates regulatory modules controlling leaf angle and provides gene editing targets for creating optimal maize architecture suitable for dense planting.


Subject(s)
Quantitative Trait Loci , Zea mays , Organogenesis, Plant , Plant Leaves/genetics , Transcription Factors/genetics , Zea mays/genetics
15.
Plant Physiol ; 188(1): 425-441, 2022 01 20.
Article in English | MEDLINE | ID: mdl-34730809

ABSTRACT

Highly efficient tissue repair is pivotal for surviving damage-associated stress. Plants generate callus upon injury to heal wound sites, yet regulatory mechanisms of tissue repair remain elusive. Here, we identified WUSCHEL-RELATED HOMEOBOX 13 (WOX13) as a key regulator of callus formation and organ adhesion in Arabidopsis (Arabidopsis thaliana). WOX13 belongs to an ancient subclade of the WOX family, and a previous study shows that WOX13 orthologs in the moss Physcomitrium patens (PpWOX13L) are involved in cellular reprogramming at wound sites. We found that the Arabidopsis wox13 mutant is totally defective in establishing organ reconnection upon grafting, suggesting that WOX13 is crucial for tissue repair in seed plants. WOX13 expression rapidly induced upon wounding, which was partly dependent on the activity of an AP2/ERF transcription factor, WOUND-INDUCED DEDIFFERENTIATION 1 (WIND1). WOX13 in turn directly upregulated WIND2 and WIND3 to further promote cellular reprogramming and organ regeneration. We also found that WOX13 orchestrates the transcriptional induction of cell wall-modifying enzyme genes, such as GLYCOSYL HYDROLASE 9Bs, PECTATE LYASE LIKEs and EXPANSINs. Furthermore, the chemical composition of cell wall monosaccharides was markedly different in the wox13 mutant. These data together suggest that WOX13 modifies cell wall properties, which may facilitate efficient callus formation and organ reconnection. Furthermore, we found that PpWOX13L complements the Arabidopsis wox13 mutant, suggesting that the molecular function of WOX13 is partly conserved between mosses and seed plants. This study provides key insights into the conservation and functional diversification of the WOX gene family during land plant evolution.


Subject(s)
Arabidopsis/growth & development , Arabidopsis/genetics , Cell Wall/physiology , Genes, Homeobox , Organogenesis, Plant/genetics , Regeneration/genetics , Gene Expression Regulation, Plant , Genes, Plant , Genetic Variation , Genotype
16.
Plant Physiol ; 188(3): 1563-1585, 2022 03 04.
Article in English | MEDLINE | ID: mdl-34986267

ABSTRACT

Arabidopsis (Arabidopsis thaliana) root hairs develop as long tubular extensions from the rootward pole of trichoblasts and exert polarized tip growth. The establishment and maintenance of root hair polarity is a complex process involving the local apical production of reactive oxygen species generated by A. thaliana nicotinamide adenine dinucleotide phosphate (NADPH) oxidase respiratory burst oxidase homolog protein C/ROOT HAIR-DEFECTIVE 2 (AtRBOHC/RHD2). Loss-of-function root hair defective 2 (rhd2) mutants have short root hairs that are unable to elongate by tip growth, and this phenotype is fully complemented by GREEN FLUORESCENT PROTEIN (GFP)-RHD2 expressed under the RHD2 promoter. However, the spatiotemporal mechanism of AtRBOHC/RHD2 subcellular redistribution and delivery to the plasma membrane (PM) during root hair initiation and tip growth are still unclear. Here, we used advanced microscopy for detailed qualitative and quantitative analysis of vesicular compartments containing GFP-RHD2 and characterization of their movements in developing bulges and growing root hairs. These compartments, identified by an independent molecular marker mCherry-VTI12 as the trans-Golgi network (TGN), deliver GFP-RHD2 to the apical PM domain, the extent of which corresponds with the stage of root hair formation. Movements of TGN/early endosomes, but not late endosomes, were affected in the bulging domains of the rhd2-1 mutant. Finally, we revealed that structural sterols might be involved in the accumulation, docking, and incorporation of TGN compartments containing GFP-RHD2 to the apical PM of root hairs. These results help in clarifying the mechanism of polarized AtRBOHC/RHD2 targeting, maintenance, and recycling at the apical PM domain, coordinated with different developmental stages of root hair initiation and growth.


Subject(s)
Arabidopsis/growth & development , Arabidopsis/genetics , Cell Membrane/metabolism , Organogenesis, Plant/genetics , Plant Roots/growth & development , Plant Roots/genetics , Trichomes/growth & development , Cell Membrane/genetics , Gene Expression Regulation, Plant , Genes, Plant , Genetic Variation , Genotype , Mutation , Trichomes/genetics
17.
Plant Physiol ; 188(1): 490-508, 2022 01 20.
Article in English | MEDLINE | ID: mdl-34726761

ABSTRACT

Somatic embryogenesis (SE) represents the most appropriate tool for next-generation breeding methods in woody plants such as grapevine (Vitis vinifera L.). However, in this species, the SE competence is strongly genotype-dependent and the molecular basis of this phenomenon is poorly understood. We explored the genetic and epigenetic basis of SE in grapevine by profiling the transcriptome, epigenome, and small RNAome of undifferentiated, embryogenic, and non-embryogenic callus tissues derived from two genotypes differing in competence for SE, Sangiovese and Cabernet Sauvignon. During the successful formation of embryonic callus, we observed the upregulation of epigenetic-related transcripts and short interfering RNAs in association with DNA hypermethylation at transposable elements in both varieties. Nevertheless, the switch to nonembryonic development matched the incomplete reinforcement of transposon silencing, and the evidence of such effect was more apparent in the recalcitrant Cabernet Sauvignon. Transcriptomic differences between the two genotypes were maximized already at early stage of culture where the recalcitrant variety expressed a broad panel of genes related to stress responses and secondary metabolism. Our data provide a different angle on the SE molecular dynamics that can be exploited to leverage SE as a biotechnological tool for fruit crop breeding.


Subject(s)
Adaptation, Physiological/genetics , Epigenomics , Organogenesis, Plant/genetics , Seeds/growth & development , Seeds/genetics , Vitis/growth & development , Vitis/genetics , Cells, Cultured , Crops, Agricultural/genetics , Crops, Agricultural/growth & development , Gene Expression Profiling , Gene Expression Regulation, Plant , Genes, Plant , Genetic Variation , Genotype , Plant Somatic Embryogenesis Techniques
18.
Plant Physiol ; 190(3): 1699-1714, 2022 10 27.
Article in English | MEDLINE | ID: mdl-35929094

ABSTRACT

The transcription factor NODULE INCEPTION (NIN) has been studied extensively for its multiple roles in root nodule symbiosis within plants of the nitrogen-fixing clade (NFC) that associate with soil bacteria, such as rhizobia and Frankia. However, NIN homologs are present in plants outside the NFC, suggesting a role in other developmental processes. Here, we show that the biofuel crop Populus sp., which is not part of the NFC, contains eight copies of NIN with diversified protein sequence and expression patterns. Lipo-chitooligosaccharides (LCOs) are produced by rhizobia and a wide range of fungi, including mycorrhizal ones, and act as symbiotic signals that promote lateral root formation. RNAseq analysis of Populus sp. treated with purified LCO showed induction of the PtNIN2 subfamily. Moreover, the expression of PtNIN2b correlated with the formation of lateral roots and was suppressed by cytokinin treatment. Constitutive expression of PtNIN2b overcame the inhibition of lateral root development by cytokinin under high nitrate conditions. Lateral root induction in response to LCOs likely represents an ancestral function of NIN retained and repurposed in nodulating plants, as we demonstrate that the role of NIN in LCO-induced root branching is conserved in both Populus sp. and legumes. We further established a visual marker of LCO perception in Populus sp. roots, the putative sulfotransferase PtSS1 that can be used to study symbiotic interactions with the bacterial and fungal symbionts of Populus sp.


Subject(s)
Populus , Rhizobium , Populus/genetics , Populus/metabolism , Gene Expression Regulation, Plant , Plant Proteins/genetics , Plant Proteins/metabolism , Organogenesis, Plant , Symbiosis , Chitin/metabolism , Cytokinins , Plant Roots/metabolism
19.
Plant Physiol ; 188(1): 220-240, 2022 01 20.
Article in English | MEDLINE | ID: mdl-34730814

ABSTRACT

Stunted growth in saline conditions is a signature phenotype of the Arabidopsis SALT OVERLY SENSITIVE mutants (sos1-5) affected in pathways regulating the salt stress response. One of the mutants isolated, sos4, encodes a kinase that phosphorylates pyridoxal (PL), a B6 vitamer, forming the important coenzyme pyridoxal 5'-phosphate (PLP). Here, we show that sos4-1 and more recently isolated alleles are deficient in phosphorylated B6 vitamers including PLP. This deficit is concomitant with a lowered PL level. Ionomic profiling of plants under standard laboratory conditions (without salt stress) reveals that sos4 mutants are perturbed in mineral nutrient homeostasis, with a hyperaccumulation of transition metal micronutrients particularly in the root, accounting for stress sensitivity. This is coincident with the accumulation of reactive oxygen species, as well as enhanced lignification and suberization of the endodermis, although the Casparian strip is intact and functional. Further, micrografting shows that SOS4 activity in the shoot is necessary for proper root development. Growth under very low light alleviates the impairments, including salt sensitivity, suggesting that SOS4 is important for developmental processes under moderate light intensities. Our study provides a basis for the integration of SOS4 derived B6 vitamers into plant health and fitness.


Subject(s)
Arabidopsis/growth & development , Organogenesis, Plant/genetics , Plant Roots/growth & development , Plant Shoots/growth & development , Pyridoxal Phosphate/genetics , Pyridoxal Phosphate/metabolism , Salt Stress/genetics , Salt Tolerance/genetics , Arabidopsis/genetics , Gene Expression Regulation, Plant , Genes, Plant , Genetic Variation , Genotype , Mutation , Plant Roots/genetics , Plant Shoots/genetics
20.
J Exp Bot ; 74(20): 6269-6284, 2023 10 31.
Article in English | MEDLINE | ID: mdl-37343125

ABSTRACT

Endoreduplication is the major source of somatic endopolyploidy in higher plants, and leads to variation in cell ploidy levels due to iterative rounds of DNA synthesis in the absence of mitosis. Despite its ubiquitous occurrence in many plant organs, tissues, and cells, the physiological meaning of endoreduplication is not fully understood, although several roles during plant development have been proposed, mostly related to cell growth, differentiation, and specialization via transcriptional and metabolic reprogramming. Here, we review recent advances in our knowledge of the molecular mechanisms and cellular characteristics of endoreduplicated cells, and provide an overview of the multi-scale effects of endoreduplication on supporting growth in plant development. In addition, the effects of endoreduplication in fruit development are discussed, since it is highly prominent during fruit organogenesis where it acts as a morphogenetic factor supporting rapid fruit growth, as illustrated by case of the model fleshy fruit, tomato (Solanum lycopersicum).


Subject(s)
Endoreduplication , Fruit , Organogenesis, Plant/genetics , Cell Cycle , Mitosis
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