Advances in Regulation of Anther Tapetum Development under Temperature Stress

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

Abstract

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

NIE Jia, LIN Hui-zi, TANG Zhe-yuan, CHEN Li-yu. Advances in Regulation of Anther Tapetum Development under Temperature Stress[J]. Biotechnology Bulletin, doi: 10.13560/j.cnki.biotech.bull.1985.2026-0046.

Figures/Tables 5

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

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

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］}

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

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

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