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Key Message <p><Emphasis Type="BoldItalic">HaEXLA2</Emphasis> <b>and</b> <Emphasis Type="BoldItalic">HaEXLB2</Emphasis> <b>enhance drought tolerance but suppress lignin defense, increasing broomrape susceptibility, revealing a trade-off in sunflowers.</b></p> Abstract <p>Expansins modulate cell wall dynamics to mediate plant stress responses. This study presents the first genome-wide analysis of the expansin gene-family in the sunflower (<i>Helianthus annuus</i>) and sunflower broomrape (<i>Orobanche cumana</i>) pathosystem, identifying 51&#xa0;<i>HaEXP</i>&#xa0;and 23&#xa0;<i>OcEXP</i>&#xa0;genes<i>.</i> Phylogenetic classification placed them into four canonical subfamilies: expansin A (EXPA), expansin B (EXPB), expansin-like A (EXLA), and expansin-like B (EXLB). The family's expansion was primarily driven by tandem duplication events under strong purifying selection. Promoter cis-element analysis revealed a high abundance of stress-responsive elements, predicting roles in ABA, JA, and hypoxia signaling. RNA-seq and RT-qPCR validation demonstrated that <i>HaEXLA2</i>&#xa0;and&#xa0;<i>HaEXLB2</i>&#xa0;were distinctly upregulated in resistant sunflowers during early&#xa0;<i>O. cumana</i>&#xa0;parasitization. Contrary to expectations, functional characterization revealed that their transient overexpression&#xa0;suppressed the phenylpropanoid pathway, downregulating key lignin biosynthetic genes (<i>PAL1, 4CL2, COMT,</i> and <i>CAD1</i>) and reducing lignin accumulation. This suppression of lignin-based defense&#xa0;significantly increased the susceptibility&#xa0;of otherwise resistant sunflower cultivars to broomrape. In parallel, heterologous expression of&#xa0;<i>HaEXLA2</i>&#xa0;and&#xa0;<i>HaEXLB2</i>&#xa0;in yeast enhanced drought tolerance by modulating cell wall properties. Our findings reveal a critical trade-off:&#xa0;<i>HaEXLA2</i>&#xa0;and&#xa0;<i>HaEXLB2</i>&#xa0;enhance abiotic stress adaptation while simultaneously suppressing lignin-based biotic defense against a root parasite. This dual functionality suggests them as potential targets for engineering stress resilience, though their negative impact on parasite resistance must be addressed in applied breeding programs.</p>

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Genome-wide analysis of sunflower (Helianthus annuus) and Orobanche cumana reveals HaEXLA2 and HaEXLB2 as negative regulators of lignin-based resistance

  • 期刊论文

  • 发表日期：

    2026年5月7日

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  • Lei Shen,
  • Yi Duan,
  • Ying Li,
  • Wenya Zhang,
  • Yan Fu,
  • Ting Zhou,
  • Hongju Sun,
  • Ahsan Ayyaz,
  • Ling Xu

摘要

Key Message

HaEXLA2 and HaEXLB2 enhance drought tolerance but suppress lignin defense, increasing broomrape susceptibility, revealing a trade-off in sunflowers.

Abstract

Expansins modulate cell wall dynamics to mediate plant stress responses. This study presents the first genome-wide analysis of the expansin gene-family in the sunflower (Helianthus annuus) and sunflower broomrape (Orobanche cumana) pathosystem, identifying 51 HaEXP and 23 OcEXP genes. Phylogenetic classification placed them into four canonical subfamilies: expansin A (EXPA), expansin B (EXPB), expansin-like A (EXLA), and expansin-like B (EXLB). The family's expansion was primarily driven by tandem duplication events under strong purifying selection. Promoter cis-element analysis revealed a high abundance of stress-responsive elements, predicting roles in ABA, JA, and hypoxia signaling. RNA-seq and RT-qPCR validation demonstrated that HaEXLA2 and HaEXLB2 were distinctly upregulated in resistant sunflowers during early O. cumana parasitization. Contrary to expectations, functional characterization revealed that their transient overexpression suppressed the phenylpropanoid pathway, downregulating key lignin biosynthetic genes (PAL1, 4CL2, COMT, and CAD1) and reducing lignin accumulation. This suppression of lignin-based defense significantly increased the susceptibility of otherwise resistant sunflower cultivars to broomrape. In parallel, heterologous expression of HaEXLA2 and HaEXLB2 in yeast enhanced drought tolerance by modulating cell wall properties. Our findings reveal a critical trade-off: HaEXLA2 and HaEXLB2 enhance abiotic stress adaptation while simultaneously suppressing lignin-based biotic defense against a root parasite. This dual functionality suggests them as potential targets for engineering stress resilience, though their negative impact on parasite resistance must be addressed in applied breeding programs.