Time-ordered co-expression network analysis reveals b-locus-mediated transcriptional cascades underlying sugarcane resistance to smut fungus (Sporisorium scitamineum)
- 1Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences/Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs/Key Laboratory of Sugarcane Genetic Improvement (Guangxi)
- 2Guangxi South Subtropical Agricultural Science Research Institute
Abstract
Sugarcane smut, caused by the biotrophic fungus Sporisorium scitamineum , causes serious yield and sugar losses. Growing resistant varieties is the main control method. The fungal b mating-type locus ( b -locus) is required for filamentous growth and virulence, but how it shapes the host response is not well understood. Here, we compared a resistant cultivar (GT29) and a susceptible cultivar (GT11-80) after inoculation with a wild-type (WT) strain or a b -locus deletion mutant, with sampling from 0 to 7 days postinoculation (dpi). We measured bE gene copy number by quantitative PCR (qPCR), assayed defense enzymes and phytohormones, and performed RNA sequencing followed by time-ordered gene co-expression network (TO-GCN) analysis. The WT strain proliferated rapidly in GT11-80 but was strongly restricted in GT29, and the b -locus mutant reached much lower levels than the WT strain in GT11-80 by 7 dpi. GT29 showed a stronger and more sustained oxidative burst (O ₂ ⁻ and H ₂ O ₂ ) than GT11-80 and maintained higher antioxidant enzyme activities. For hormones, WT infection induced more jasmonic acid (JA) and 1-aminocyclopropane-1-carboxylic acid (ACC; the ethylene precursor) than the mutant, with the highest levels in GT29 at 5 dpi, whereas salicylic acid (SA) accumulated late (7 dpi) in GT11-80; abscisic acid (ABA) stayed high under WT infection but dropped under the mutant. TO-GCN analysis identified a WT-specific, time-ordered transcription factor (TF) cascade in GT11-80 that was lost under mutant infection, whereas the GT29 network kept its temporal order under both conditions. In the jasmonic acid/ethylene (JA/ET) subnetwork, ERF1 was a central hub in GT11-80, while in GT29 ERF1 was much less connected and EIN3 was the main hub. Overall, the b -locus is required for the time-ordered transcriptional response during infection, and the resistant and susceptible cultivars differ in their hormone dynamics and JA/ET network structure. These findings provide candidate genes and network features for breeding smut-resistant sugarcane.
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BibTeX
@article{song2026timeordered,
title = {{Time-ordered co-expression network analysis reveals b-locus-mediated transcriptional cascades underlying sugarcane resistance to smut fungus (Sporisorium scitamineum)}},
author = {Xiu-Peng Song and Xiao-Qiu Zhang and Bing-Qiang Lu and Dong-Mei Huang and Yong-Jian Liang and Bao-Qing Zhang and Yu-Chi Deng and Dong-Mei Li and Yang-Rui Li and Qiang Liang and Krishan K. Verma and Mei-Xin Yan},
journal = {Frontiers in Plant Science},
year = {2026},
month = oct,
doi = {10.3389/fpls.2026.1929311},
url = {https://www.frontiersin.org/articles/10.3389/fpls.2026.1929311/full},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Time-ordered co-expression network analysis reveals b-locus-mediated transcriptional cascades underlying sugarcane resistance to smut fungus (Sporisorium scitamineum)
AU - Xiu-Peng Song
AU - Xiao-Qiu Zhang
AU - Bing-Qiang Lu
AU - Dong-Mei Huang
AU - Yong-Jian Liang
AU - Bao-Qing Zhang
AU - Yu-Chi Deng
AU - Dong-Mei Li
AU - Yang-Rui Li
AU - Qiang Liang
AU - Krishan K. Verma
AU - Mei-Xin Yan
PY - 2026
DA - 2026/10/16
JO - Frontiers in Plant Science
DO - 10.3389/fpls.2026.1929311
UR - https://www.frontiersin.org/articles/10.3389/fpls.2026.1929311/full
AB - Sugarcane smut, caused by the biotrophic fungus Sporisorium scitamineum , causes serious yield and sugar losses. Growing resistant varieties is the main control method. The fungal b mating-type locus ( b -locus) is required for filamentous growth and virulence, but how it shapes the host response is not well understood. Here, we compared a resistant cultivar (GT29) and a susceptible cultivar (GT11-80) after inoculation with a wild-type (WT) strain or a b -locus deletion mutant, with sampling from 0 to 7 days postinoculation (dpi). We measured bE gene copy number by quantitative PCR (qPCR), assayed defense enzymes and phytohormones, and performed RNA sequencing followed by time-ordered gene co-expression network (TO-GCN) analysis. The WT strain proliferated rapidly in GT11-80 but was strongly restricted in GT29, and the b -locus mutant reached much lower levels than the WT strain in GT11-80 by 7 dpi. GT29 showed a stronger and more sustained oxidative burst (O ₂ ⁻ and H ₂ O ₂ ) than GT11-80 and maintained higher antioxidant enzyme activities. For hormones, WT infection induced more jasmonic acid (JA) and 1-aminocyclopropane-1-carboxylic acid (ACC; the ethylene precursor) than the mutant, with the highest levels in GT29 at 5 dpi, whereas salicylic acid (SA) accumulated late (7 dpi) in GT11-80; abscisic acid (ABA) stayed high under WT infection but dropped under the mutant. TO-GCN analysis identified a WT-specific, time-ordered transcription factor (TF) cascade in GT11-80 that was lost under mutant infection, whereas the GT29 network kept its temporal order under both conditions. In the jasmonic acid/ethylene (JA/ET) subnetwork, ERF1 was a central hub in GT11-80, while in GT29 ERF1 was much less connected and EIN3 was the main hub. Overall, the b -locus is required for the time-ordered transcriptional response during infection, and the resistant and susceptible cultivars differ in their hormone dynamics and JA/ET network structure. These findings provide candidate genes and network features for breeding smut-resistant sugarcane.
SN - 1664-462X
ER -