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

Title: Cell‐ and development‐specific degradation controls the levels of mixed‐linkage glucan in sorghum leaves

Journal Article · · The Plant Journal
DOI: https://doi.org/10.1111/tpj.16376 · OSTI ID:1992542
ORCiD logo [1];  [2];  [3];  [2];  [2];  [3]; ORCiD logo [1]
  1. Great Lakes Bioenergy Research Center Michigan State University East Lansing Michigan 48824 USA, MSU‐DOE Plant Research Laboratory Michigan State University East Lansing Michigan 48824 USA, Department of Plant Biology Michigan State University East Lansing Michigan 48824 USA
  2. Great Lakes Bioenergy Research Center Michigan State University East Lansing Michigan 48824 USA, MSU‐DOE Plant Research Laboratory Michigan State University East Lansing Michigan 48824 USA
  3. Great Lakes Bioenergy Research Center Michigan State University East Lansing Michigan 48824 USA, Department of Biochemistry and Biophysics Texas A&,M University College Station Texas 77845 USA

SUMMARY Mixed‐linkage glucan (MLG) is a component of the cell wall (CW) of grasses and is composed of glucose monomers linked by β‐1,3 and β‐1,4 bonds. MLG is believed to have several biological functions, such as the mobilizable storage of carbohydrates and structural support of the CW. The extracellular levels of MLG are largely controlled by rates of synthesis mediated by cellulose synthase‐like (CSL) enzymes, and turnover by lichenases. Economically important crops like sorghum accumulate MLG to variable levels during development. While in sorghum, like other grasses, there is one major MLG synthase (CSLF6), the identity of lichenases is yet unknown. To fill this gap, we identified three sorghum lichenases (SbLCH1‐3) and characterized them in leaves in relation to the expression of SbCSLF6 , and the abundance of MLG and starch. We established that SbLCH1‐3 are secreted to the apoplast, consistent with a role of degrading MLG extracellularly. Furthermore, while SbCSLF6 expression was associated with cell development, the SbLCH genes exhibited distinct development‐, cell‐type‐specific and diel‐regulated expression. Therefore, our study identifies three functional sorghum MLG lichenases and highlights that MLG accumulation in sorghum leaves is likely controlled by the activity of lichenases that tune MLG levels, possibly to suit distinct cell and developmental needs in planta . These findings have important implications for improving the growth, yield, and composition of sorghum as a feedstock.

Research Organization:
Michigan State Univ., East Lansing, MI (United States); Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC)
Grant/Contract Number:
FG02-91ER20021; SC0018409
OSTI ID:
1992542
Journal Information:
The Plant Journal, Journal Name: The Plant Journal Journal Issue: 2 Vol. 116; ISSN 0960-7412
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (46)

Designing sorghum as a dedicated bioenergy feedstock journal October 2007
Over-expression of (1,3;1,4)- β -D-glucanase isoenzyme EII gene results in decreased (1,3;1,4)- β -D-glucan content and increased starch level in barley grains: (1,3;1,4)- β - d -Glucan content and starch level in barley grains journal April 2016
Purification and characterization of (1?3, 1?4)-?-glucan endohydrolases from germinated wheat (Triticum aestivum) journal August 1993
Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles journal April 2005
Substrate specificities and kinetic properties of two (1→3), (1→4)-β-d-glucan endo-hydrolases from germinating barley (Hordeum vulgare) journal August 1982
Expression of an endo-(1,3;1,4)-β-glucanase in response to wounding, methyl jasmonate, abscisic acid and ethephon in rice seedlings journal November 2009
Leaf growth in dicots and monocots: so different yet so alike journal October 2016
Characterization of the primary cell walls of seedlings of Brachypodium distachyon – A potential model plant for temperate grasses journal January 2010
Maize and sorghum: genetic resources for bioenergy grasses journal August 2008
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads journal February 2015
Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein journal November 2004
Uncovering pH at both sides of the root plasma membrane interface using noninvasive imaging journal June 2018
Synthesis of (1-->3), (1-->4)-beta-D-glucan in the Golgi apparatus of maize coleoptiles. journal May 1993
The rapid generation of mutation data matrices from protein sequences journal January 1992
Energy Sorghum--a genetic model for the design of C4 grass bioenergy crops journal June 2014
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms journal May 2018
(1,3;1,4)-β-D-Glucans in Cell Walls of the Poaceae, Lower Plants, and Fungi: A Tale of Two Linkages journal September 2009
Advances in Cell Wall Matrix Research with a Focus on Mixed-Linkage Glucan journal July 2021
A mixed-linkage (1,3;1,4)-β-D-glucan specific hydrolase mediates dark-triggered degradation of this plant cell wall polysaccharide journal January 2021
The Genetics and Transcriptional Profiles of the Cellulose Synthase-Like HvCslF Gene Family in Barley journal February 2008
Development of Cellulosic Secondary Walls in Flax Fibers Requires β-Galactosidase       journal May 2011
Loss of Cellulose Synthase - Like F6 Function Affects Mixed-Linkage Glucan Deposition, Cell Wall Mechanical Properties, and Defense Responses in Vegetative Tissues of Rice journal March 2012
Cell Wall and Membrane-Associated Exo-β-d-Glucanases from Developing Maize Seedlings journal June 2000
Chemical Structure of the Cell Walls of Dwarf Maize and Changes Mediated by Gibberellin journal November 1988
β-d-Glucan Antibodies Inhibit Auxin-Induced Cell Elongation and Changes in the Cell Wall of Zea Coleoptile Segments journal August 1989
Developmental Regulation of (1→3, 1→4)-β-Glucanase Gene Expression in Barley: Tissue-Specific Expression of Individual Isoenzymes journal July 1992
Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth journal January 1993
Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins journal January 2008
Cell-wall carbohydrates and their modification as a resource for biofuels journal May 2008
Sugar treatment inhibits IAA-induced expression of endo-1,3:1,4-β-glucanase EI transcripts in barley coleoptile segments journal April 2010
Purification and Chemical Properties of Two 1,3;1,4-beta-Glucan Endohydrolases from Germinating Barley journal January 1982
Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1,3;1,4)-β-d-glucans and alters their fine structure: Over-expression of CslF genes in barley journal January 2011
Distribution, structure and biosynthetic gene families of (1,3;1,4)-β-glucan in Sorghum bicolor : (1,3;1,4)-β-glucan in journal March 2015
Dynamics of biomass partitioning, stem gene expression, cell wall biosynthesis, and sucrose accumulation during development of Sorghum bicolor journal September 2016
The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization journal December 2017
The AGCVIII kinase Dw2 modulates cell proliferation, endomembrane trafficking, and MLG/xylan cell wall localization in elongating stem internodes of Sorghum bicolor journal December 2020
Disruption of Brachypodium lichenase alters metabolism of mixed‐linkage glucan and starch journal December 2021
Mechanism of mixed-linkage glucan biosynthesis by barley cellulose synthase–like CslF6 (1,3;1,4)-β-glucan synthase journal November 2022
Expression profiling and integrative analysis of the CESA/CSL superfamily in rice journal January 2010
ER stress signaling requires RHD3, a functionally conserved ER-shaping GTPase journal May 2014
Differences in protein structural regions that impact functional specificity in GT2 family β-glucan synthases journal October 2019
Source-to-sink transport of sugar and regulation by environmental factors journal January 2013
Evaluation of Sorghum [Sorghum bicolor (L.)] Reference Genes in Various Tissues and under Abiotic Stress Conditions for Quantitative Real-Time PCR Data Normalization journal April 2016
Characterisation of Cellulose Synthase Like F6 (CslF6) Mutants Shows Altered Carbon Metabolism in β-D-(1,3;1,4)-Glucan Deficient Grain in Brachypodium distachyon journal January 2021
The root apoplastic pH as an integrator of plant signaling journal August 2022
Mixed-Linkage Glucan Is the Main Carbohydrate Source and Starch Is an Alternative Source during Brachypodium Grain Germination journal April 2023