DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Bioenergy sorghum nodal root bud development: morphometric, transcriptomic and gene regulatory network analysis

Journal Article · · Frontiers in Plant Science

Bioenergy sorghum’s large and deep nodal root system and associated microbiome enables uptake of water and nutrients from and deposition of soil organic carbon into soil profiles, key contributors to the crop’s resilience and sustainability. The goal of this study was to increase our understanding of bioenergy sorghum nodal root bud development. Sorghum nodal root bud initiation was first observed on the stem node of the 7th phytomer below the shoot apex. Buds were initiated near the upper end of the stem node pulvinus on the side of the stem opposite the tiller bud, then additional buds were added over the next 6-8 days forming a ring of 10-15 nascent nodal root buds around the stem. Later in plant development, a second ring of nodal root buds began forming on the 17th stem node immediately above the first ring of buds. Overall, nodal root bud development can take ~40 days from initiation to onset of nodal root outgrowth. Nodal root buds were initiated in close association with vascular bundles in the rind of the pulvinus. Stem tissue forming nascent nodal root buds expressed sorghum homologs of genes associated with root initiation (WOX4), auxin transport (LAX2, PIN4), meristem activation (NGAL2), and genes involved in cell proliferation. Expression of WOX11 and WOX5, genes involved in root stem niche formation, increased early in nodal root bud development followed by genes encoding PLTs, LBDs (LBD29), LRP1, SMB, RGF1 and root cap LEAs later in development. A nodal root bud gene regulatory network module expressed during nodal root bud initiation predicted connections linking PFA5, SPL9 and WOX4 to genes involved in hormone signaling, meristem activation, and cell proliferation. A network module expressed later in development predicted connections among SOMBRERO, a gene involved in root cap formation, and GATA19, BBM, LBD29 and RITF1/RGF1 signaling. Overall, this study provides a detailed description of bioenergy sorghum nodal root bud development and transcriptome information useful for understanding the regulation of sorghum nodal root bud formation and development.

Research Organization:
Board of Regents of the University of Wisconsin System, operating as University of Wisconsin-Madison; Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)
Grant/Contract Number:
SC0018409
OSTI ID:
2506748
Journal Information:
Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 15; ISSN 1664-462X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (127)

High biomass yield energy sorghum: developing a genetic model for C4 grass bioenergy crops: Modeling and Analysis: Developing a genetic model for C4 grass bioenergy crops journal September 2012
Designing sorghum as a dedicated bioenergy feedstock journal October 2007
Proteomic analysis of shoot-borne root initiation in maize (Zea mays L.) journal April 2006
Bioenergy Underground: Challenges and opportunities for phenotyping roots and the microbiome for sustainable bioenergy crop production journal January 2022
Auxin and root initiation in somatic embryos of Arabidopsis journal July 2006
Strigolactone Positively Controls Crown Root Elongation in Rice journal August 2011
LBD13 positively regulates lateral root formation in Arabidopsis journal January 2019
ATHB17 Is a Positive Regulator of Abscisic Acid Response during Early Seedling Growth journal February 2013
Morphological and architectural development of root systems in sorghum and maize journal March 2010
Yield Results and Stability Analysis from the Sorghum Regional Biomass Feedstock Trial journal March 2014
Genotype-Environment-Management Interactions in Biomass Yield and Feedstock Composition of Photoperiod-Sensitive Energy Sorghum journal March 2021
Dissecting Arabidopsis lateral root development journal April 2003
Energy sorghum hybrids: Functional dynamics of high nitrogen use efficiency journal September 2013
The role of ABA and MAPK signaling pathways in plant abiotic stress responses journal January 2014
Phyllotaxis and Rhizotaxis in Arabidopsis Are Modified by Three PLETHORA Transcription Factors journal June 2013
Programmed Cell Death Controlled by ANAC033/SOMBRERO Determines Root Cap Organ Size in Arabidopsis journal May 2014
Identification of Conserved Gene-Regulatory Networks that Integrate Environmental Sensing and Growth in the Root Cambium journal August 2020
Pluripotent Pericycle Cells Trigger Different Growth Outputs by Integrating Developmental Cues into Distinct Regulatory Modules journal November 2020
A cellular analysis of meristem activity at the end of flowering points to cytokinin as a major regulator of proliferative arrest in Arabidopsis journal February 2022
The NAC Domain Transcription Factors FEZ and SOMBRERO Control the Orientation of Cell Division Plane in Arabidopsis Root Stem Cells journal December 2008
Establishment of Expression in the SHORTROOT-SCARECROW Transcriptional Cascade through Opposing Activities of Both Activators and Repressors journal December 2016
Transcription factor LkWOX4 is involved in adventitious root development in Larix kaempferi journal October 2020
MapMan4: A Refined Protein Classification and Annotation Framework Applicable to Multi-Omics Data Analysis journal June 2019
The role of auxin transporters and receptors in adventitious rooting of Arabidopsis thaliana pre-etiolated flooded seedlings journal January 2020
The WUSCHEL-related homeobox transcription factor OsWOX4 controls the primary root elongation by activating OsAUX1 in rice journal September 2020
AINTEGUMENTA-LIKE proteins: hubs in a plethora of networks journal March 2014
A Model for Nitrogen Fixation in Cereal Crops journal March 2020
The rice FLATTENED SHOOT MERISTEM, encoding CAF-1 p150 subunit, is required for meristem maintenance by regulating the cell-cycle period journal July 2008
AtPIN4 Mediates Sink-Driven Auxin Gradients and Root Patterning in Arabidopsis journal March 2002
Simulated Biomass Sorghum GHG Reduction Potential is Similar to Maize journal August 2020
The business case for soil journal March 2017
RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana journal May 2016
PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development journal October 2007
MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor journal March 2010
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads journal February 2015
ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells journal January 2015
HISAT: a fast spliced aligner with low memory requirements journal March 2015
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources journal December 2008
Transcriptional regulatory framework for vascular cambium development in Arabidopsis roots journal October 2019
Two types of bHLH transcription factor determine the competence of the pericycle for lateral root initiation journal May 2021
RGF1 controls root meristem size through ROS signalling journal December 2019
Early post-embryonic root formation is specifically affected in the maize mutantlrt1 journal October 1998
LATERAL BRANCHING OXIDOREDUCTASEacts in the final stages of strigolactone biosynthesis inArabidopsis journal May 2016
Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds journal December 2016
Soil carbon debt of 12,000 years of human land use journal August 2017
PLETHORA transcription factors orchestrate de novo organ patterning during Arabidopsis lateral root outgrowth journal October 2017
Arabidopsis TSO1 and MYB3R1 form a regulatory module to coordinate cell proliferation with differentiation in shoot and root journal March 2018
bHLH093/NFL and bHLH061 are required for apical meristem function in Arabidopsis thaliana journal July 2018
Genetic Dissection of Root Formation in Maize (Zea mays) Reveals Root-type Specific Developmental Programmes journal February 2004
Analysis of the arabidopsis REM gene family predicts functions during flower development journal July 2014
AINTEGUMENTA and AINTEGUMENTA-LIKE6 directly regulate floral homeotic, growth, and vascular development genes in young Arabidopsis flowers journal May 2021
At the root of quiescence: function and regulation of the quiescent center journal June 2021
Hormonal orchestration of root apical meristem formation and maintenance in Arabidopsis journal August 2021
Energy Sorghum--a genetic model for the design of C4 grass bioenergy crops journal June 2014
Arabidopsis ADF5 promotes stomatal closure by regulating actin cytoskeleton remodeling in response to ABA and drought stress journal November 2018
DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update) journal March 2022
PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants journal November 2018
Mucilage on the Root Surface and Root Hairs of Sorghum: Heterogeneity in Structure, Manner of Production and Site of Accumulation journal July 1978
Arrest, Senescence and Death of Shoot Apical Stem Cells inArabidopsis thaliana journal November 2022
MOROKOSHI: Transcriptome Database in Sorghum bicolor journal December 2014
De novo stem cell establishment in meristems requires repression of organ boundary cell fate journal August 2022
Essential roles of SERKs in the ROOT MERISTEM GROWTH FACTOR-mediated signaling pathway journal February 2022
Auxin Control of Root Development journal April 2010
LBD18/ASL20Regulates Lateral Root Formation in Combination withLBD16/ASL18Downstream ofARF7andARF19in Arabidopsis journal August 2009
WOX4 Promotes Procambial Development journal December 2009
SHORT-ROOT Regulates Primary, Lateral, and Adventitious Root Development in Arabidopsis journal October 2010
Localized Induction of the ATP-Binding Cassette B19 Auxin Transporter Enhances Adventitious Root Formation in Arabidopsis journal May 2013
The Physiology of Adventitious Roots journal December 2015
Transcription Factors WOX11/12 Directly Activate WOX5/7 to Promote Root Primordia Initiation and Organogenesis journal October 2016
Identification of Players Controlling Meristem Arrest Downstream of the FRUITFULL-APETALA2 Pathway journal August 2020
Crown rootless1 , Which Is Essential for Crown Root Formation in Rice, Is a Target of an AUXIN RESPONSE FACTOR in Auxin Signaling journal April 2005
The WUSCHEL-Related Homeobox Gene WOX11 Is Required to Activate Shoot-Borne Crown Root Development in Rice journal March 2009
AUX/LAX Genes Encode a Family of Auxin Influx Transporters That Perform Distinct Functions during Arabidopsis Development journal July 2012
WUSCHEL-RELATED HOMEOBOX4Is Involved in Meristem Maintenance and Is Negatively Regulated by the CLE GeneFCP1in Rice journal January 2013
ANGUSTIFOLIA3 Binds to SWI/SNF Chromatin Remodeling Complexes to Regulate Transcription during Arabidopsis Leaf Development journal January 2014
WOX11 and 12 Are Involved in the First-Step Cell Fate Transition during de Novo Root Organogenesis in Arabidopsis journal March 2014
The Ubiquitous Distribution of Late Embryogenesis Abundant Proteins across Cell Compartments in Arabidopsis Offers Tailored Protection against Abiotic Stress journal July 2014
BEL1-LIKE HOMEODOMAIN6 and KNOTTED ARABIDOPSIS THALIANA7 Interact and Regulate Secondary Cell Wall Formation via Repression of REVOLUTA journal December 2014
Axillary Meristem Formation in Rice Requires the WUSCHEL Ortholog TILLERS ABSENT1 journal April 2015
Dynamic Changes in ANGUSTIFOLIA3 Complex Composition Reveal a Growth Regulatory Mechanism in the Maize Leaf journal June 2015
Rice Homeodomain Protein WOX11 Recruits a Histone Acetyltransferase Complex to Establish Programs of Cell Proliferation of Crown Root Meristem journal May 2017
GIF Transcriptional Coregulators Control Root Meristem Homeostasis journal January 2018
LRP1, a gene expressed in lateral and adventitious root primordia of arabidopsis. journal June 1995
Sorghum biomass production in the continental United States and its potential impacts on soil organic carbon and nitrous oxide emissions journal August 2020
Ecosystem‐scale biogeochemical fluxes from three bioenergy crop candidates: How energy sorghum compares to maize and miscanthus journal December 2020
Bioenergy sorghum’s deep roots: A key to sustainable biomass production on annual cropland journal December 2021
Total carbon and nitrogen in the soils of the world journal June 1996
Fasga: A new polychromatic method for simultaneous and differential staining of plant tissues journal October 1987
The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation: Map-based cloning of the maize RTCS gene journal April 2007
C4 Plants as Biofuel Feedstocks: Optimising Biomass Production and Feedstock Quality from a Lignocellulosic PerspectiveFree Access journal January 2011
Cooperative action of the paralogous maize lateral organ boundaries (LOB) domain proteins RTCS and RTCL in shoot‐borne root formation journal April 2015
Divide et impera: boundaries shape the plant body and initiate new meristems journal September 2015
WUSCHEL ‐ RELATED HOMEOBOX 4 ( WOX 4) ‐like genes regulate cambial cell division activity and secondary growth in Populus trees journal June 2017
XYLEM NAC DOMAIN1, an angiosperm NAC transcription factor, inhibits xylem differentiation through conserved motifs that interact with RETINOBLASTOMA-RELATED journal July 2017
Moving on up – controlling internode growth journal February 2020
Deconstructing the root system of grasses through an exploration of development, anatomy and function journal February 2022
Transcription factors PRE 3 and WOX 11 are involved in the formation of new lateral roots from secondary growth taproot in A. thaliana journal March 2018
Soil carbon improvement under long‐term (36 years) no‐till sorghum production in a sub‐tropical environment journal September 2020
Auxin responsiveness of the MONOPTEROS-BODENLOS module in primary root initiation critically depends on the nuclear import kinetics of the Aux/IAA inhibitor BODENLOS journal January 2016
The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization journal December 2017
Auxin signaling modulates LATERAL ROOT PRIMORDIUM1 (LRP1) expression during lateral root development in Arabidopsis journal October 2019
Bioenergy sorghum stem growth regulation: intercalary meristem localization, development, and gene regulatory network analysis journal September 2022
Secreted Peptide Signals Required for Maintenance of Root Stem Cell Niche in Arabidopsis journal August 2010
A conserved superlocus regulates above- and belowground root initiation journal March 2022
The nodal roots of Zea : their development in relation to structural features of the stem journal November 1986
Strigolactones, a Novel Carotenoid-Derived Plant Hormone journal April 2015
WGCNA: an R package for weighted correlation network analysis journal December 2008
Molecular Mechanisms of Root Development in Rice journal January 2019
LBD16 and LBD18 acting downstream of ARF7 and ARF19 are involved in adventitious root formation in Arabidopsis journal January 2019
Histological quantification of maize stem sections from FASGA-stained images journal November 2017
UMAP: Uniform Manifold Approximation and Projection journal September 2018
Adventitious Root Development from the Coleoptilar Node in Zea mays L. journal July 1976
Identification of Nitrogen-Fixing Bradyrhizobium Associated With Roots of Field-Grown Sorghum by Metagenome and Proteome Analyses journal March 2019
Getting to the roots of it: Genetic and hormonal control of root architecture journal January 2013
Bioenergy Sorghum Crop Model Predicts VPD-Limited Transpiration Traits Enhance Biomass Yield in Water-Limited Environments journal March 2017
Auxin Control of Root Organogenesis from Callus in Tissue Culture journal August 2017
The YUCCA-Auxin-WOX11 Module Controls Crown Root Development in Rice journal April 2018
Cell Type-Specific Transcriptomics of Lateral Root Formation and Plasticity journal February 2019
Lateral Root Primordium Morphogenesis in Angiosperms journal March 2019
Transcriptional Regulation of Sorghum Stem Composition: Key Players Identified Through Co-expression Gene Network and Comparative Genomics Analyses journal March 2020
Control of Root Stem Cell Differentiation and Lateral Root Emergence by CLE16/17 Peptides in Arabidopsis journal April 2022
Epicuticular wax accumulation and regulation of wax pathway gene expression during bioenergy Sorghum stem development journal October 2023
Arabidopsis Hypocotyl Adventitious Root Formation Is Suppressed by ABA Signaling journal July 2021
Cereal Grass Pulvini: Agronomically Significant Models for Studying Gravitropism Signaling and Tissue Polarity journal January 2013
Long-term bioenergy sorghum harvest strategy and soil quality journal January 2016
SCARECROW reinforces SHORT-ROOT signaling and inhibits periclinal cell divisions in the ground tissue by maintaining SHR at high levels in the endodermis journal December 2012
Molecular Cloning, Phylogenetic Analysis, Expressional Profiling and In Vitro Studies of TINY2 from Arabidopsis thaliana journal July 2005