Bioenergy sorghum stem growth regulation: intercalary meristem localization, development, and gene regulatory network analysis

Abstract

SUMMARY Bioenergy sorghum is a highly productive drought tolerant C4 grass that accumulates 80% of its harvestable biomass in approximately 4 m length stems. Stem internode growth is regulated by development, shading, and hormones that modulate cell proliferation in intercalary meristems (IMs). In this study, sorghum stem IMs were localized above the pulvinus at the base of elongating internodes using magnetic resonance imaging, microscopy, and transcriptome analysis. A change in cell morphology/organization occurred at the junction between the pulvinus and internode where LATERAL ORGAN BOUNDARIES (SbLOB), a boundary layer gene, was expressed. Inactivation of an AGCVIII kinase in DDYM (dw2) resulted in decreased SbLOB expression, disrupted IM localization, and reduced internode cell proliferation. Transcriptome analysis identified approximately 1000 genes involved in cell proliferation, hormone signaling, and other functions selectively upregulated in the IM compared with a non‐meristematic stem tissue. This cohort of genes is expressed in apical dome stem tissues before localization of the IM at the base of elongating internodes. Gene regulatory network analysis identified connections between genes involved in hormone signaling and cell proliferation. The results indicate that gibberellic acid induces accumulation of growth regulatory factors (GRFs) known to interact with ANGUSTIFOLIA (SbAN3), a master regulator of cell proliferation. GRF:AN3 was predicted to induce SbARF3/ETT expression and regulate SbAN3 expression in an auxin‐dependent manner. GRFs and ARFs regulate genes involved in cytokinin and brassinosteroid signaling and cell proliferation. The results provide a molecular framework for understanding how hormone signaling regulates the expression of genes involved in cell proliferation in the stem IM.

Unveiling shared genetic regulators for plant architectural and biomass yield traits in sorghum

“…Additionally, several growth regulators, such as phytohormones, play an important role in plant growth and development, contributing to biomass. For instance, auxin and brassinosteroid are associated with height (Hirano et al, 2017;Upadhyaya et al, 2013;Mu et al, 2022), while gibberellin and cytokinin are linked to stem biomass and diameter (Wang et al, 2020;Wang et al, 2022;Yu et al, 2022).…”

Cell‐type‐specific transcriptomics uncovers spatial regulatory networks in bioenergy sorghum stems

“…Sorghum stem growth is regulated in a complex way by development (McKinley et al, 2016), auxin transport (Multani et al, 2003), brassinosteroid signaling (Hilley et al, 2016;Hirano et al, 2017), an AGCVIII kinase (Oliver et al, 2021), gibberellin (Ordonio et al, 2014), and shade avoidance signaling (Yu et al, 2021). Phytomers generated by the shoot apical meristem/rib meristem initially produce leaves followed by the activation of the stem intercalary meristem at the upper end of the pulvinus that generates cells required for stem internode growth (Yu et al, 2022). Cells generated by the intercalary meristem subsequently elongate and then vascular bundle sclerenchyma cells and epidermal cells accumulate secondary cell walls (SCWs) increasing the mechanical strength of the stem (Kebrom et al, 2017;Yu et al, 2022).…”

“…Phytomers generated by the shoot apical meristem/rib meristem initially produce leaves followed by the activation of the stem intercalary meristem at the upper end of the pulvinus that generates cells required for stem internode growth (Yu et al, 2022). Cells generated by the intercalary meristem subsequently elongate and then vascular bundle sclerenchyma cells and epidermal cells accumulate secondary cell walls (SCWs) increasing the mechanical strength of the stem (Kebrom et al, 2017;Yu et al, 2022). Transcriptional regulation of the sorghum stem SCW pathway has been investigated through analysis of stem tissues collected at various stages of sorghum development (Hennet et al, 2020).…”

The stem cell-type transcriptome of bioenergy sorghum reveals the spatial regulation of secondary cell wall networks

“…Sorghum stem growth is regulated in a complex way by development (McKinley et al, 2016), auxin transport (Multani et al, 2003), brassinosteroid signaling (Hilley et al, 2016;Hirano et al, 2017), an AGCVIII kinase (Oliver et al, 2021), gibberellin (Ordonio et al, 2014), and shade avoidance signaling (Yu et al, 2021). Phytomers generated by the shoot apical meristem/rib meristem initially produce leaves followed by the activation of the stem intercalary meristem at the upper end of the pulvinus that generates cells required for stem internode growth (Yu et al, 2022). Cells generated by the intercalary meristem subsequently elongate and then xylem sclerenchyma cells and epidermal cells accumulate secondary cell walls (SCWs) that help prevent stalk breakage (Kebrom et al, 2017;Yu et al, 2022).…”

“…Phytomers generated by the shoot apical meristem/rib meristem initially produce leaves followed by the activation of the stem intercalary meristem at the upper end of the pulvinus that generates cells required for stem internode growth (Yu et al, 2022). Cells generated by the intercalary meristem subsequently elongate and then xylem sclerenchyma cells and epidermal cells accumulate secondary cell walls (SCWs) that help prevent stalk breakage (Kebrom et al, 2017;Yu et al, 2022). Transcriptional regulation of the sorghum stem SCW pathway has been investigated through analysis of stem tissues collected at various stages of sorghum development (Hennet et al, 2020).…”