拟南芥MAP18调控花粉管生长方向的机理研究
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摘要
花粉管是一种进行快速极性生长的细胞。花粉落到柱头上后,经历了萌发和极性生长,生长的花粉管受到胚珠信号的吸引通过珠孔进入胚珠,释放精细胞,从而完成双受精过程。花粉管的正常生长是保证双受精过程可以正常完成的必要条件,同时花粉管也是研究植物细胞生长调控机制的重要模式细胞。因此,研究花粉管的生长具有很重要的意义。
MAP18((Microtubule-Associated Protein18)是本实验室最早报道的一个DREPP家族的微管结合蛋白,可以使微管去稳定,调控拟南芥细胞的各向异性生长。基因芯片的分析数据表明MAP18在拟南芥花粉及花粉管中的表达量是全株中最高的,但是还没有关于MAP18在花粉及花粉管中功能的报道,因此开展了本论文的研究。
通过表型观察发现,虽然突变体map18的萌发率与野生型相同,但map18和MAP18OX花粉管均表现出生长方向发生异常的表型。体外萌发的map18的花粉管发生偏转,MAP18OX花粉管表现为弯曲波动且其程度与MAP18的表达量呈正相关。在体内萌发、生长的map18和MAP18OX花粉管均表现出扭曲和环绕胚珠生长的现象,并且有些花粉管由于其生长方向的异常导致了进入胚珠失败,从而造成了结实率下降。通过正反交实验证明了,map18和MAP18OX花粉管生长方向异常的表型与母本无关。这说明了MAP18对于调控花粉管的生长方向具有重要功能。
为了说明MAP18控制花粉管生长方向的机制,对map18和MAP18OX花粉管内细胞骨架的组织方式和动态进行了观察,发现虽然MAP18表达量的改变不影响花粉管内微管骨架的组织方式,但是MAP18通过调控花粉管顶端及亚顶端区内微丝的组织方式和动态,从而影响了其生长方向。体外生化功能分析显示,MAP18具有依赖Ca2+的切割微丝的活性,并且MAP18的第1和2个V-E-E-K-K基序对于其切割微丝的活性十分重要。通过对表达MAP18点突变蛋白的植株的表型观察分析发现：MAP18是通过其Ca2+依赖性的切割微丝的活性来调控花粉管顶端及亚顶端的微丝动态,从而控制花粉管的生长方向。
此外,通过对MAP18promoter:MAP18-eGFP花粉管观察发现,MAP18在花粉管中的定位是与花粉管的生长状态相关的。MAP18在伸长生长的花粉管在胫部区域主要定位于细胞质膜,而在顶端和亚顶端区域则无细胞质膜的定位。而当花粉管停止生长时MAP18在花粉管中主要定位于整个细胞质膜,包括顶端和亚顶端区域。恢复生长后MAP18又会从顶端和亚顶端区的质膜上消失。这表明MAP18在正常生长的花粉管中的定位模式是维持花粉管生长所必需的。但是,MAP18的Ca2+依赖性的切割微丝的活性变化并不影响其在伸长生长花粉管中的亚细胞定位。
本学位论文的研究结果证明MAP18是一个新的控制花粉管生长方向的重要调控因子,MAP18通过其Ca2+依赖性的微丝切割活性参与调控花粉管的生长方向。此前对花粉管生长的研究多集中于对花粉管生长速率的调控机制,而对花粉管生长方向调控机制的研究较少。本论文的研究不仅鉴定到新的调控花粉管生长方向的调控因子,同时也证明了对微丝动态的调控不仅作用于花粉管生长速率的控制,同时也作用于花粉管生长方向的控制。本论文对MAP18调控花粉管生长方向机制的研究对于全面阐明花粉管生长调控的机理具有重要的科学理论意义。
Pollen tube growth is a rapid and polarized process that occurs exclusively at the tube tip. The elongation of pollen tubes within the female reproductive tissues is crucial for delivering sperm cells to ovules for fertilization. In addition, the growth of pollen tubes is a model system for studying polarized cell expansion or tip growth.
Previously report has demonstrated that Arabidopsis thaliana Microtubule-Associated Protein18(MAP18) belongs to a DREPP family and regulates cortical microtubule organization by destabilizing microtubules. Bioinformation analysis indicates that MAP18is expressed highly in pollen and pollen tubes. However, there is no report about whether MAP18is involved in pollen tube growth yet. The investigation was therefore carried out in this thesis.
Observations showed no obvious differences in germination or pollen tube elongation rate between wild type and mapl8mutant, suggesting that MAP18might not function in these processes. However, mapl8pollen tubes displayed abnormal growth patterns, with swollen tips and bending growth in vitro. In vivo observations also indicated that both mapl8and MAP18OX pollen tubes displayed entangled, sporadic growth patterns in the transmitting tracts, sometimes failing to reach the ovules and resulted in reduced micropyle targeting. These observations demonstrated that MAP18is involved in the regulation of the direction of pollen tube growth in Arabidopsis.
To demonstrate the mechanism how MAP18regulates the direction of pollen tube growth, the cytoskeleton of map18and MAP18OX pollen tubes was observed. Althought no obvious changes of the microtubule cytoskeleton was observed in map18pollen tubes, the organization and dynamics of F-actin in the apical and subapical regions were siginificantly altered in growing map18and MAP18OX pollen tubes. These results suggest that MAP18functions in F-actin organization and dynamics in the apical and subapical regions. Biochemical analysis indicated that MAP18bound to and severed actin filaments in a Ca2+-dependent manner in vitro. Expressing the point mutation proteins of MAP18in map18pollen tubes demonstrated that the F-actin-severing activity of MAP18is critical for appropriate growth patterns of pollen tubes.
In addition, observations showed that MAP18localized to the plasma membrane in the flank region but not in the the apical and subapical regions of growing pollen tubes. However, MAP18localized to whole plasma membrane in non-growing pollen tubes, but disappeared from the apical plasma membrane when tube growth was restarted. These observations indicated that the subcellular localization of MAP18is important for the function of MAP18.
These results revealed that MAP18functions as a key factor involved in controlling the direction of pollen tube growth by severing F-actin, and suggesting that regulations of the organization and dynamic of F-actin is important not only for the pollen tube growth but also for the control of the direction of pollen tube growth. This study demonstrates a new function of MAP18that involved in controlling the direction of pollen tube growth and provides insights into the mechanism that controls the direction of pollen tube growth based on the F-actin-severing activity of MAP18.
MAP18((Microtubule-Associated Protein18)是本实验室最早报道的一个DREPP家族的微管结合蛋白,可以使微管去稳定,调控拟南芥细胞的各向异性生长。基因芯片的分析数据表明MAP18在拟南芥花粉及花粉管中的表达量是全株中最高的,但是还没有关于MAP18在花粉及花粉管中功能的报道,因此开展了本论文的研究。
通过表型观察发现,虽然突变体map18的萌发率与野生型相同,但map18和MAP18OX花粉管均表现出生长方向发生异常的表型。体外萌发的map18的花粉管发生偏转,MAP18OX花粉管表现为弯曲波动且其程度与MAP18的表达量呈正相关。在体内萌发、生长的map18和MAP18OX花粉管均表现出扭曲和环绕胚珠生长的现象,并且有些花粉管由于其生长方向的异常导致了进入胚珠失败,从而造成了结实率下降。通过正反交实验证明了,map18和MAP18OX花粉管生长方向异常的表型与母本无关。这说明了MAP18对于调控花粉管的生长方向具有重要功能。
为了说明MAP18控制花粉管生长方向的机制,对map18和MAP18OX花粉管内细胞骨架的组织方式和动态进行了观察,发现虽然MAP18表达量的改变不影响花粉管内微管骨架的组织方式,但是MAP18通过调控花粉管顶端及亚顶端区内微丝的组织方式和动态,从而影响了其生长方向。体外生化功能分析显示,MAP18具有依赖Ca2+的切割微丝的活性,并且MAP18的第1和2个V-E-E-K-K基序对于其切割微丝的活性十分重要。通过对表达MAP18点突变蛋白的植株的表型观察分析发现：MAP18是通过其Ca2+依赖性的切割微丝的活性来调控花粉管顶端及亚顶端的微丝动态,从而控制花粉管的生长方向。
此外,通过对MAP18promoter:MAP18-eGFP花粉管观察发现,MAP18在花粉管中的定位是与花粉管的生长状态相关的。MAP18在伸长生长的花粉管在胫部区域主要定位于细胞质膜,而在顶端和亚顶端区域则无细胞质膜的定位。而当花粉管停止生长时MAP18在花粉管中主要定位于整个细胞质膜,包括顶端和亚顶端区域。恢复生长后MAP18又会从顶端和亚顶端区的质膜上消失。这表明MAP18在正常生长的花粉管中的定位模式是维持花粉管生长所必需的。但是,MAP18的Ca2+依赖性的切割微丝的活性变化并不影响其在伸长生长花粉管中的亚细胞定位。
本学位论文的研究结果证明MAP18是一个新的控制花粉管生长方向的重要调控因子,MAP18通过其Ca2+依赖性的微丝切割活性参与调控花粉管的生长方向。此前对花粉管生长的研究多集中于对花粉管生长速率的调控机制,而对花粉管生长方向调控机制的研究较少。本论文的研究不仅鉴定到新的调控花粉管生长方向的调控因子,同时也证明了对微丝动态的调控不仅作用于花粉管生长速率的控制,同时也作用于花粉管生长方向的控制。本论文对MAP18调控花粉管生长方向机制的研究对于全面阐明花粉管生长调控的机理具有重要的科学理论意义。
Pollen tube growth is a rapid and polarized process that occurs exclusively at the tube tip. The elongation of pollen tubes within the female reproductive tissues is crucial for delivering sperm cells to ovules for fertilization. In addition, the growth of pollen tubes is a model system for studying polarized cell expansion or tip growth.
Previously report has demonstrated that Arabidopsis thaliana Microtubule-Associated Protein18(MAP18) belongs to a DREPP family and regulates cortical microtubule organization by destabilizing microtubules. Bioinformation analysis indicates that MAP18is expressed highly in pollen and pollen tubes. However, there is no report about whether MAP18is involved in pollen tube growth yet. The investigation was therefore carried out in this thesis.
Observations showed no obvious differences in germination or pollen tube elongation rate between wild type and mapl8mutant, suggesting that MAP18might not function in these processes. However, mapl8pollen tubes displayed abnormal growth patterns, with swollen tips and bending growth in vitro. In vivo observations also indicated that both mapl8and MAP18OX pollen tubes displayed entangled, sporadic growth patterns in the transmitting tracts, sometimes failing to reach the ovules and resulted in reduced micropyle targeting. These observations demonstrated that MAP18is involved in the regulation of the direction of pollen tube growth in Arabidopsis.
To demonstrate the mechanism how MAP18regulates the direction of pollen tube growth, the cytoskeleton of map18and MAP18OX pollen tubes was observed. Althought no obvious changes of the microtubule cytoskeleton was observed in map18pollen tubes, the organization and dynamics of F-actin in the apical and subapical regions were siginificantly altered in growing map18and MAP18OX pollen tubes. These results suggest that MAP18functions in F-actin organization and dynamics in the apical and subapical regions. Biochemical analysis indicated that MAP18bound to and severed actin filaments in a Ca2+-dependent manner in vitro. Expressing the point mutation proteins of MAP18in map18pollen tubes demonstrated that the F-actin-severing activity of MAP18is critical for appropriate growth patterns of pollen tubes.
In addition, observations showed that MAP18localized to the plasma membrane in the flank region but not in the the apical and subapical regions of growing pollen tubes. However, MAP18localized to whole plasma membrane in non-growing pollen tubes, but disappeared from the apical plasma membrane when tube growth was restarted. These observations indicated that the subcellular localization of MAP18is important for the function of MAP18.
These results revealed that MAP18functions as a key factor involved in controlling the direction of pollen tube growth by severing F-actin, and suggesting that regulations of the organization and dynamic of F-actin is important not only for the pollen tube growth but also for the control of the direction of pollen tube growth. This study demonstrates a new function of MAP18that involved in controlling the direction of pollen tube growth and provides insights into the mechanism that controls the direction of pollen tube growth based on the F-actin-severing activity of MAP18.
引文
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