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Drought is associated with inhibition of pollen tube directional growth via enhancing nitric oxide signaling in Gossypium hirsutum ovules

Jiyuan Miao1*, Mengdie Cheng1*, Wajid Ali Khattak2, Zhanhan Wang1, Huilian Yu1 ,Wenqing Zhao1, Shanshan Wang1, Binglin Chen1, Youhua Wang1, Zhiguo Zhou1, Qiuxiang Tang3#, Wei Hu1#

1 College of Agriculture, Nanjing Agricultural University, Nanjing 210095, China

2 College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China

3 College of Agronomy, Xinjiang Agricultural University, Urumqi 830052, China

  Highlights  

Drought disrupts pollen tube guidance via nitric oxide accumulation at the ovular micropyle, leading to fertilization failure

Drought stress increased the relative expression of GhNIAD and NR activity in the ovules of both cotton cultivars, promoting the conversion of NO2- to NO.

The reduction in GSNOR activity under drought conditions inhibited the breakdown of GSNO, maintaining higher NO levels in the ovules.

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摘要  

干旱胁迫已被报道会损害花粉管在雌蕊中的趋化性生长,但其在陆地棉(Gossypium hirsutum)中的生理机制尚未得到探究。本研究提出假设:干旱诱导的胚珠一氧化氮(NO)变化可能抑制花粉管的定向生长。为验证上述假设,本研究选用两个棉花品种——豫早棉9110(干旱敏感型)和德夏棉1号(干旱耐受型)在水分胁迫下进行池栽试验。结果表明,干旱胁迫抑制了花粉管向胚囊的定向生长,同时降低了受精率、单铃棉籽数及单铃重。此外,相关性分析显示,胚珠中NO含量与受精率呈显著负相关,暗示胚珠中NO的变化可能抑制花粉管定向生长及后续产量构成因素的形成。进一步分析表明,干旱胁迫提高了两个品种胚珠中硝酸还原酶(NR)的活性,促进亚硝酸盐(NO₂⁻)向NO的转化。这一过程伴随着两个品种干旱胁迫胚珠中NR基因(GhNIAD)表达的上调,进一步促进了NO的合成。干旱条件下S-亚硝基谷胱甘肽还原酶(GSNOR)活性的降低与S-亚硝基谷胱甘肽(GSNO)的积累相关,表明NO清除能力减弱导致胚珠中NO水平升高。此外,NO水平的升高可能作为一种调控机制,进一步抑制干旱胁迫下两个品种胚珠中GSNOR的活性。因此,这些研究结果揭示,干旱导致棉花胚珠中NO积累,这可能是抑制花粉管生长的因素之一。当然,这一因果关系有待未来研究提供更多证据予以确认。本研究为揭示水分亏缺引发棉花生殖障碍的分子-生理机制提供了新见解。



Abstract  

Drought stress has been reported to impair chemotropism of pollen tube growth in the pistil, yet the physiological mechanisms underlying this phenomenon remain unexplored in G. hirsutum. This study hypothesized that drought-induced nitric oxide (NO) changes in ovules may inhibit pollen tube directional growth. To test the above hypothesis, pools experiments were conducted using two cotton (Gossypium hirsutum L.) cultivars Yuzaomian 9110 (drought-sensitive) and Dexiamian 1 (drought-tolerant) under water stress. Results demonstrated that drought stress inhibited the directional growth of pollen tube to the embryo sac and simultaneously reduced fertilization rate, the number of cotton seeds per boll as well as the single boll weight. Moreover, correlation analyses showed that NO content in the ovules had significantly negative correlation with the fertilization rate, implying that NO changes in ovules might inhibit pollen tube directional growth and subsequent yield component formation. Further analyses showed that drought stress elevated nitrate reductase (NR) activity in the ovules of both cultivars, facilitating the conversion of nitrite (NO2-) to NO. This process was accompanied by the up-regulation of NR gene (GhNIAD) expressions in the drought-affected ovules of both cultivars, further promoting NO synthesis. The reduction in S-nitrosoglutathione reductase (GSNOR) activity under drought conditions was correlated with an accumulation of S-nitrosoglutathione (GSNO), suggesting that the compromised removal of NO contributed to the higher NO levels in the ovules. Additionally, elevated NO levels may, as part of a regulatory mechanism, further inhibit the activity of GSNOR in the ovules of both cultivars under drought stress. Thus, these findings revealed that drought leads to the accumulation of NO in the cotton ovules, which may be a factor inhibiting pollen tube growth. Of course, this causal relationship requires more evidence to be confirmed in future research. These results provide novel insights into the molecular-physiological mechanisms by which water deficit triggers reproductive failure in cotton.

Keywords:  cotton       water deficit       NO       pollen tube growth              in vivo  
Online: 23 January 2026  
Fund: This work was supported by the Key Research and Development Program of Xinjiang, China (2024B02004-3), the National Natural Science Foundation of China (32272223 and 32572464), the China Agriculture Research System of MOF and MARA (CARS-15-14 and CARS-15-13), the Collaborative Innovation Center for Modern Crop Production co-sponsored by Province and Ministry, China (CIC-MCP).
About author:  #Correspondence Wei Hu, E-mail: weihu@njau.edu.cn; Qiuxiang Tang, E-mail: tangqiuxiang2004_2@163.com * These authors contributed equally to this paper.

Cite this article: 

Jiyuan Miao, Mengdie Cheng, Wajid Ali Khattak, Zhanhan Wang, Huilian Yu , Wenqing Zhao, Shanshan Wang, Binglin Chen, Youhua Wang, Zhiguo Zhou, Qiuxiang Tang, Wei Hu. 2026. Drought is associated with inhibition of pollen tube directional growth via enhancing nitric oxide signaling in Gossypium hirsutum ovules. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.01.030

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