温度胁迫调控花药绒毡层发育的研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2026-0046

摘要/Abstract

摘要：

近年来，随着全球气候变暖的加剧，极端天气频发，温度胁迫显著影响花粉育性，给农业生产带来巨大损失。绒毡层是位于花药壁内层的分泌细胞，不仅为小孢子发育提供必需的营养物质，还为花粉外壁的形成提供原料。在花药发育过程中，绒毡层细胞会经历程序性细胞死亡（programmed cell death, PCD），这一过程的提前或延迟均会导致花粉败育。现有研究表明，高温通常会导致绒毡层PCD的提前，而低温则可能抑制或延迟其发生。在此过程中往往伴随着活性氧（reactive oxygen species, ROS）的过度积累及激素信号紊乱，同时影响内质网（endoplasmic reticulum, ER）的结构及功能，导致大量错误折叠及未折叠蛋白质积累。温度胁迫还可能直接影响蛋白质的降解以破坏蛋白质稳态。此外，花药绒毡层发育及降解的遗传模块DYT1-TDF1-AMS-MYB80-MS1在响应温度胁迫时也发挥着重要作用。本文综述了绒毡层细胞在高低温胁迫下的表型特征，总结了高低温如何通过调控绒毡层DYT1-TDF1-AMS-MYB80-MS1转录激活级联通路的表达，破坏ROS、内质网和蛋白质稳态，以及引起激素信号紊乱来干扰绒毡层发育及PCD时序，进而影响花粉育性。此外，本文还讨论了在有性生殖阶段研究温度胁迫对花粉育性影响的挑战，并展望相关研究在作物育种和农业生产中的潜在应用价值，包括培育耐高低温品种、丰富作物抗逆基因库、优化栽培管理策略、研发新型化学药剂等方面。

关键词: 温度胁迫, 绒毡层, 程序性细胞死亡, 花粉育性, 活性氧, 激素信号, 内质网应激, 蛋白质稳态

Abstract:

With the escalation of global warming, extreme weather events have become more frequent, leading to temperature stress that severely compromises pollen fertility and results in significant agricultural losses. The tapetum, consisting of secretory cells located in the inner wall of the anther, provides vital nutrients for microspore development and materials essential for pollen exine formation. During anther development, tapetum cells undergo programmed cell death (PCD); deviations in the timing of this process, whether premature or delayed, can lead to pollen sterility. Recent studies indicate that high temperatures primarily trigger early PCD in tapetum cells, whereas low temperatures tend to inhibit or delay it. This process is often accompanied by excessive accumulation of reactive oxygen species (ROS) and hormone signaling disruption. Additionally, temperature stress induces structural and functional abnormalities in the endoplasmic reticulum (ER), resulting in massive accumulation of misfolded and unfolded proteins. Temperature stress can also directly disrupt protein homeostasis by interfering with protein degradation. Furthermore, the genetic module DYT1-TDF1-AMS-MYB80-MS1, which regulates the development and degradation of the anther tapetum, also plays an important role in responding to temperature stress. In this review, we examine the phenotypic characteristics of tapetal cells under high and low temperature stress, and summarize how these stresses regulate the expression of the tapetal DYT1-TDF1-AMS-MYB80-MS1 transcriptional activation cascade. This regulation disrupts the homeostasis of ROS, ER and proteins, and triggers phytohormone signaling disruption, interfering with tapetal development and the timing of PCD, ultimately affecting pollen fertility. In addition, we discuss the challenges of studying the effects of temperature stress on pollen fertility during the sexual reproductive phase of plants, and explore the potential applications of these studies in crop breeding and agricultural production. These applications include breeding temperature-tolerant cultivars, enriching crop stress resistance gene pools, optimizing cultivation management strategies, and developing novel chemical regulators.

Key words: temperature stress, tapetum, programmed cell death, pollen fertility, reactive oxygen species, hormone signaling, endoplasmic reticulum stress, proteostasis

聂佳, 林慧子, 唐哲源, 陈立余. 温度胁迫调控花药绒毡层发育的研究进展[J]. 生物技术通报, 2026, 42(9): 14-28.

NIE Jia, LIN Hui-zi, TANG Zhe-yuan, CHEN Li-yu. Advances in Regulation of Anther Tapetum Development under Temperature Stress[J]. Biotechnology Bulletin, 2026, 42(9): 14-28.

图/表 5

图1 phyA/B介导温度调控绒毡层发育及花粉育性温度胁迫通过SlphyA/SlphyB-SlPIF4信号调节SlDYT1-SlTDF1-SlAMS-SlMYB80-SlMS1级联反应，改变绒毡层PCD，使其在高温下加速降解或在低温下延迟降解，从而导致花粉败育

Fig. 1 phyA/B-mediated temperature regulation of tapetum development and pollen fertilityTemperature stress modulates the SlDYT1-SlTDF1-SlAMS-SlMYB80-SlMS1 cascade via SlphyA/SlphyB-SlPIF4 signaling, altering tapetum PCD, accelerating its degradation under heat stress or delaying it under cold stress, leading to pollen abortion

图2 高温与低温胁迫对ROS稳态的影响低温胁迫诱导ROS上调，水稻中OsCTB6与CATA相互作用，在低温下维持CATA的稳定，对ROS进行清除。低温胁迫下ROS的过量积累会导致ROS稳态被破坏，可能导致绒毡层PCD延迟。高温胁迫提高OsRBOH活性，促进ROS爆发，SOD、POD和CAT活性降低，导致ROS过早积累，使绒毡层PCD提前。箭头：促进；T型杆：抑制；虚线：机制尚未完全阐明

Fig. 2 The influence of high and low temperature stress on ROS homeostasisLow temperature stress induces the upregulation of reactive oxygen species (ROS). In rice, OsCTB6 interacts with CATA to maintain CATA stability under cold conditions and eliminate excess ROS. Excessive ROS accumulation under cold stress disrupts ROS homeostasis, thereby potentially delaying tapetal programmed cell death (PCD). By contrast, high temperature stress enhances OsRBOH activity and triggers ROS burst, accompanied by reduced activities of SOD, POD and CAT. This results in premature ROS accumulation and advanced tapetal PCD. Arrows: Promotion; T-bars: inhibition; dashed lines: mechanisms not yet fully elucidated

表1 高温与低温胁迫影响绒毡层PCD的核心差异

Table 1 Core differences in the impact of high and low temperature stress on tapetal PCD

对比维度 Comparative aspects	高温胁迫 High temperature stress	低温胁迫 Low temperature stress
细胞学表型 Cytological phenotype	核心特征为绒毡层PCD提前启动、过早降解。四分体至单核小孢子早期就启动PCD，绒毡层提前解体，细胞层变薄甚至消失，细胞中液泡增多甚至液泡膜破裂、内质网异常、线粒体肿胀、胼胝质增厚及沉积异常^{［21，41-44］}	核心特征为绒毡层PCD显著延迟、降解受阻。PCD启动时间大幅推迟，降解进程被抑制，细胞持续留存至花粉成熟期，出现绒毡层肿胀及细胞肥大、液泡化异常、内质网结构异常、胼胝质降解提前^{［32-34，38-39，44］}
转录级联调控模式 Regulatory pattern of the transcriptional cascade	主要抑制DYT1-TDF1-AMS-MYB80转录级联通路基因的表达，加速绒毡层PCD进程^{［110-111］}	主要异常增强DYT1-TDF1-AMS-MYB80级联通路的转录活性，如低温下SlPIF4与SlDYT1形成复合体，显著增强SlTDF1的转录激活，导致绒毡层PCD信号被抑制；或直接抑制MYB80等核心基因表达，阻断PCD执行^［39］
ROS调控机制 ROS regulatory mechanism	ROS爆发主要源于线粒体呼吸链功能紊乱与ABA介导的NADPH氧化酶激活，抗氧化酶（CAT、SOD）活性被显著抑制；过量ROS直接触发绒毡层PCD提前启动，是高温下绒毡层PCD提前的核心诱因^{［73，114］}	ROS积累主要源于抗氧化酶（如CATA）的蛋白稳定性被破坏；ROS稳态被破坏^{［27，70］}
ABA调控机制 ABA regulatory mechanism	ABA水平升高通过激活ROS积累提前诱导绒毡层PCD，导致绒毡层提前降解^［73］	ABA积累通过负调控绒毡层糖代谢相关基因表达，扰乱花药中的糖分供应，介导绒毡层PCD异常^{［93，113］}

表1 高温与低温胁迫影响绒毡层PCD的核心差异

Table 1 Core differences in the impact of high and low temperature stress on tapetal PCD

对比维度 Comparative aspects	高温胁迫 High temperature stress	低温胁迫 Low temperature stress
细胞学表型 Cytological phenotype	核心特征为绒毡层PCD提前启动、过早降解。四分体至单核小孢子早期就启动PCD，绒毡层提前解体，细胞层变薄甚至消失，细胞中液泡增多甚至液泡膜破裂、内质网异常、线粒体肿胀、胼胝质增厚及沉积异常^{［21，41-44］}	核心特征为绒毡层PCD显著延迟、降解受阻。PCD启动时间大幅推迟，降解进程被抑制，细胞持续留存至花粉成熟期，出现绒毡层肿胀及细胞肥大、液泡化异常、内质网结构异常、胼胝质降解提前^{［32-34，38-39，44］}
转录级联调控模式 Regulatory pattern of the transcriptional cascade	主要抑制DYT1-TDF1-AMS-MYB80转录级联通路基因的表达，加速绒毡层PCD进程^{［110-111］}	主要异常增强DYT1-TDF1-AMS-MYB80级联通路的转录活性，如低温下SlPIF4与SlDYT1形成复合体，显著增强SlTDF1的转录激活，导致绒毡层PCD信号被抑制；或直接抑制MYB80等核心基因表达，阻断PCD执行^［39］
ROS调控机制 ROS regulatory mechanism	ROS爆发主要源于线粒体呼吸链功能紊乱与ABA介导的NADPH氧化酶激活，抗氧化酶（CAT、SOD）活性被显著抑制；过量ROS直接触发绒毡层PCD提前启动，是高温下绒毡层PCD提前的核心诱因^{［73，114］}	ROS积累主要源于抗氧化酶（如CATA）的蛋白稳定性被破坏；ROS稳态被破坏^{［27，70］}
ABA调控机制 ABA regulatory mechanism	ABA水平升高通过激活ROS积累提前诱导绒毡层PCD，导致绒毡层提前降解^［73］	ABA积累通过负调控绒毡层糖代谢相关基因表达，扰乱花药中的糖分供应，介导绒毡层PCD异常^{［93，113］}

图3 绒毡层PCD对温度胁迫响应的调控网络温度胁迫主要通过4条途径调控绒毡层PCD进程：转录级联通路、内质网与蛋白质稳态、ROS稳态以及激素信号。高温胁迫主要抑制转录级联通路相关基因表达，通过上调bZIP28/60介导UPR并促进CP蛋白积累，扰乱内质网及蛋白质稳态；在ROS稳态方面，高温抑制抗氧化酶基因表达，同时通过上调ABA、下调JA加剧ROS失衡；此外高温还会降低GA含量，最终共同促进绒毡层PCD进程。低温胁迫则促进转录级联通路基因表达，激活NAC家族转录因子参与内质网稳态调控；低温同样抑制抗氧化酶基因表达，并通过降低IAA水平导致ROS积累；同时，低温引起ABA上调、GA下调，最终共同导致绒毡层PCD进程延迟。bZIP28/60/17：bZIP转录因子家族；NAC062/NAC103/NAC089：NAC转录因子家族；UPR：未折叠蛋白反应；CP：半胱氨酸蛋白酶；GA：赤霉素；ABA：脱落酸；JA：茉莉酸；IAA：生长素；CAT：过氧化氢酶；SOD：超氧化物歧化酶；POD：过氧化物酶；APX：抗坏血酸过氧化物酶。箭头：促进；T型杆：抑制；虚线：机制尚未完全阐明；橙色线代表高温，蓝色线代表低温

Fig. 3 Regulatory network of the tapetum PCD response to temperature stressTemperature stress regulates the progression of tapetal PCD mainly through four pathways: the transcriptional cascade, ER homeostasis and proteostasis, ROS homeostasis, and hormonal signaling. High-temperature stress mainly inhibits the expression of genes involved in the transcriptional cascade. It disrupts ER homeostasis and proteostasis by upregulating bZIP28/bZIP60 to mediate the UPR, as well as promoting the accumulation of CPs. With respect to ROS homeostasis, high temperature suppresses the expression of antioxidant enzyme genes and exacerbates ROS imbalance by elevating ABA levels and reducing JA levels. In addition, high temperature decreases GA levels. Collectively, these events accelerate the progression of tapetal PCD. Low-temperature stress promotes the expression of genes in the transcriptional cascade and activates NAC family transcription factors to regulate ER homeostasis. Similarly, low temperature inhibits the expression of antioxidant enzyme genes and induces ROS accumulation by reducing IAA levels. Meanwhile, low temperature increases ABA levels and decreases GA levels, which together lead to the delay of tapetal PCD progression. bZIP28/60/17: bZIP transcription factor family members; NAC062/NAC103/NAC089: NAC transcription factor family members; UPR: unfolded protein response; CP: cysteine protease; GA: gibberellin; ABA: abscisic acid; JA: jasmonic acid; IAA: auxin; CAT: catalase; SOD: superoxide dismutase; POD: peroxidase; APX: ascorbate peroxidase. Arrows: Promotion; T-bars: inhibition; dashed lines: mechanisms not yet fully elucidated; orange line: high temperature; blue line: low temperature

图4 绒毡层细胞温度响应机制的农业应用前景

Fig. 4 Agricultural application prospects of temperature response mechanism of tapetum cells

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