<p>Soil salinization poses a critical and escalating threat to global agriculture and forestry, driving the need to understand plant salt tolerance mechanisms for sustainable cultivation on marginal lands. This study presents a comprehensive, multi-level investigation into the salt stress responses of <i>Idesia polycarpa</i> ‘Yuji’, a promising bioenergy tree species. Seedlings were subjected to a gradient of neutral mixed salt stress (NaCl: Na₂SO₄, 9:1 molar ratio) at concentrations of 50, 100, and 150 mmol·L⁻¹. Our integrated analysis revealed that salt stress progressively inhibited growth, damaged the microstructure of leaves and root tips, and severely impaired photosynthetic function, as evidenced by reduced pigment content and decreased net photosynthetic and transpiration rates. Physiological profiling showed dynamic adjustments in osmotic regulation substances, proline, soluble sugars, and soluble proteins, alongside increased malondialdehyde (MDA) accumulation, indicating membrane peroxidation under severe stress. Antioxidant enzymes responded in a time- and concentration-dependent manner, with superoxide dismutase (SOD) and peroxidase (POD) activities showing distinct activation patterns. Hormonal analysis revealed a significant reconfiguration of endogenous phytohormones, characterized by sustained elevation of abscisic acid (ABA) and nuanced changes in indole-3-acetic acid (IAA), zeatin riboside (ZR), and gibberellic acid-3 (GA₃). Transcriptome sequencing identified 8,644 differentially expressed genes (DEGs), with enrichment analyses highlighting key involvement of pathways related to photosynthesis, plant MAPK signaling, and α-linolenic acid metabolism. Critical regulatory genes within hormone signal transduction cascades, including <i>RAN1</i>, <i>MAPK6/9/17/18</i>, <i>PYR/PYL</i>, and <i>SRK2</i>, were prominently modulated, underscoring the central role of MAPK-mediated hormonal crosstalk in coordinating the acclimation response. Our findings demonstrate that <i>I. polycarpa</i> ‘Yuji’ employs a deeply integrated tolerance strategy, spanning morphological adaptation, physiological and biochemical rebalancing, and extensive transcriptional reprogramming. This study not only elucidates the mechanistic basis of salt tolerance in this undervalued species but also provides a valuable repository of candidate genes and pathways for future genetic improvement, supporting the development of resilient genotypes for the effective utilization of saline-alkaline soils.</p> Graphical Abstract <p></p> <p>Integrated response mechanism of <i>I. polycarpa</i> ‘Yuji’ to salt stress. Under salt stress, <i>I. polycarpa</i> ‘Yuji’ exhibits distinct morphological changes in leaves and roots, accompanied by alterations in key physiological and biochemical indicators. Transcriptome analysis reveals widespread transcriptional reprogramming, with significant modulation of gene families involved in hormone signaling, particularly within the MAPK cascade, and stress-responsive pathways, collectively underpinning the species’ adaptive tolerance mechanism.</p>

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Integrated Morpho-physiological and Transcriptomic Analysis Reveals the Salt Tolerance Mechanisms in Idesia Polycarpa ‘Yuji’ Seedlings

  • Qichao Xu,
  • Yinghui Yang,
  • Yanmei Wang,
  • Zhi Li,
  • Qifei Cai,
  • Xiaodong Geng,
  • Mengxing Zhang,
  • Li Dai,
  • Zhen Liu

摘要

Soil salinization poses a critical and escalating threat to global agriculture and forestry, driving the need to understand plant salt tolerance mechanisms for sustainable cultivation on marginal lands. This study presents a comprehensive, multi-level investigation into the salt stress responses of Idesia polycarpa ‘Yuji’, a promising bioenergy tree species. Seedlings were subjected to a gradient of neutral mixed salt stress (NaCl: Na₂SO₄, 9:1 molar ratio) at concentrations of 50, 100, and 150 mmol·L⁻¹. Our integrated analysis revealed that salt stress progressively inhibited growth, damaged the microstructure of leaves and root tips, and severely impaired photosynthetic function, as evidenced by reduced pigment content and decreased net photosynthetic and transpiration rates. Physiological profiling showed dynamic adjustments in osmotic regulation substances, proline, soluble sugars, and soluble proteins, alongside increased malondialdehyde (MDA) accumulation, indicating membrane peroxidation under severe stress. Antioxidant enzymes responded in a time- and concentration-dependent manner, with superoxide dismutase (SOD) and peroxidase (POD) activities showing distinct activation patterns. Hormonal analysis revealed a significant reconfiguration of endogenous phytohormones, characterized by sustained elevation of abscisic acid (ABA) and nuanced changes in indole-3-acetic acid (IAA), zeatin riboside (ZR), and gibberellic acid-3 (GA₃). Transcriptome sequencing identified 8,644 differentially expressed genes (DEGs), with enrichment analyses highlighting key involvement of pathways related to photosynthesis, plant MAPK signaling, and α-linolenic acid metabolism. Critical regulatory genes within hormone signal transduction cascades, including RAN1, MAPK6/9/17/18, PYR/PYL, and SRK2, were prominently modulated, underscoring the central role of MAPK-mediated hormonal crosstalk in coordinating the acclimation response. Our findings demonstrate that I. polycarpa ‘Yuji’ employs a deeply integrated tolerance strategy, spanning morphological adaptation, physiological and biochemical rebalancing, and extensive transcriptional reprogramming. This study not only elucidates the mechanistic basis of salt tolerance in this undervalued species but also provides a valuable repository of candidate genes and pathways for future genetic improvement, supporting the development of resilient genotypes for the effective utilization of saline-alkaline soils.

Graphical Abstract

Integrated response mechanism of I. polycarpa ‘Yuji’ to salt stress. Under salt stress, I. polycarpa ‘Yuji’ exhibits distinct morphological changes in leaves and roots, accompanied by alterations in key physiological and biochemical indicators. Transcriptome analysis reveals widespread transcriptional reprogramming, with significant modulation of gene families involved in hormone signaling, particularly within the MAPK cascade, and stress-responsive pathways, collectively underpinning the species’ adaptive tolerance mechanism.