Background <p>Global climate warming has increasingly exacerbated the adverse effects of high temperature on crop yield and quality. <i>Saccharum spontaneum</i>,<i> a wild reso</i>urce that serves as a crucial genetic reservoir for sugarcane, represents a valuable genetic asset for improving heat tolerance in sugarcane breeding. Recent studies have shown that <i>S. spontaneum contributes</i> to modern sugarcane breeding not only as a source of resistance genes but also to sugar accumulation in contemporary cultivars. However, the molecular basis underlying its photosynthetic recovery following combined heat and high light stress remains unclear.</p> Materials and methods <p>In this study, 20 <i>S. spontaneum accessions w</i>ere evaluated under natural high-temperature and high-light conditions by measuring photosynthetic parameters at 09:00, 14:00, and 17:00. Two accessions showing contrasting post-noon recovery of net photosynthetic rate were identified: the fast-recovering line 82–114 (L114) and the slow-recovering line 2021-17 (L17).</p> Results <p>Transcriptome sequencing and differential expression analyses revealed that the differentially expressed genes (DEGs) were predominantly enriched in pathways related to plant hormone signal transduction, antioxidant enzyme systems, photosynthesis, and carbon metabolism. Further weighted gene co-expression network analysis (WGCNA) identified co-expression modules highly associated with the afternoon samples of L114, along with key regulatory factors including <i>WRKY</i>,<i> NF-YC</i>,<i> CAMTA</i>,<i> C2H2</i>, and <i>RLK</i> family members. Physiological and molecular data together indicate that L114 orchestrates a dynamic response under heat and high light stress by remodeling ethylene, jasmonic acid, and auxin signaling networks; coordinately enhancing peroxisome-associated antioxidant systems; transiently downregulating and subsequently restoring the expression of light-harvesting and electron transport genes in the photosystems; and finely tuning glycolysis, the tricarboxylic acid (TCA) cycle, and the pentose phosphate pathway to achieve a temporal response characterized by “damage suppression–rapid repair–recovery of high photosynthesis.” This study is the first to investigate candidate pathways underlying the rapid recovery of photosynthesis following midday depression in <i>S. spontaneum</i>, and to identify germplasm with high photosynthetic capacity and rapid post-midday recovery. These mechanistic insights provide novel candidate targets for functional validation and genetic improvement in sugarcane breeding.</p>

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Comparative physiological and transcriptomic analysis of rapid post-midday photosynthetic recovery in Saccharum spontaneum reveals candidate pathways for sugarcane improvement

  • Maoyong Ran,
  • Ruiqian Zhou,
  • Lixuan Ge,
  • Junjie Zhao,
  • Jiahui Yang,
  • Bo Yu,
  • Weitong Zhao,
  • Yue Wang,
  • Zhiwei Yang,
  • Guoqiang Huang,
  • Liangnian Xu,
  • Chaohua Huang,
  • Jiayong Liu,
  • Zuhu Deng,
  • Xinwang Zhao

摘要

Background

Global climate warming has increasingly exacerbated the adverse effects of high temperature on crop yield and quality. Saccharum spontaneum, a wild resource that serves as a crucial genetic reservoir for sugarcane, represents a valuable genetic asset for improving heat tolerance in sugarcane breeding. Recent studies have shown that S. spontaneum contributes to modern sugarcane breeding not only as a source of resistance genes but also to sugar accumulation in contemporary cultivars. However, the molecular basis underlying its photosynthetic recovery following combined heat and high light stress remains unclear.

Materials and methods

In this study, 20 S. spontaneum accessions were evaluated under natural high-temperature and high-light conditions by measuring photosynthetic parameters at 09:00, 14:00, and 17:00. Two accessions showing contrasting post-noon recovery of net photosynthetic rate were identified: the fast-recovering line 82–114 (L114) and the slow-recovering line 2021-17 (L17).

Results

Transcriptome sequencing and differential expression analyses revealed that the differentially expressed genes (DEGs) were predominantly enriched in pathways related to plant hormone signal transduction, antioxidant enzyme systems, photosynthesis, and carbon metabolism. Further weighted gene co-expression network analysis (WGCNA) identified co-expression modules highly associated with the afternoon samples of L114, along with key regulatory factors including WRKY, NF-YC, CAMTA, C2H2, and RLK family members. Physiological and molecular data together indicate that L114 orchestrates a dynamic response under heat and high light stress by remodeling ethylene, jasmonic acid, and auxin signaling networks; coordinately enhancing peroxisome-associated antioxidant systems; transiently downregulating and subsequently restoring the expression of light-harvesting and electron transport genes in the photosystems; and finely tuning glycolysis, the tricarboxylic acid (TCA) cycle, and the pentose phosphate pathway to achieve a temporal response characterized by “damage suppression–rapid repair–recovery of high photosynthesis.” This study is the first to investigate candidate pathways underlying the rapid recovery of photosynthesis following midday depression in S. spontaneum, and to identify germplasm with high photosynthetic capacity and rapid post-midday recovery. These mechanistic insights provide novel candidate targets for functional validation and genetic improvement in sugarcane breeding.