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Low pH-induced cell wall disturbances in Arabidopsis thaliana roots lead to a pattern-specific programmed cell death in the different root zones and arrested elongation in late elongation zone
Environmental and Experimental Botany ( IF 5.7 ) Pub Date : 2021-07-30 , DOI: 10.1016/j.envexpbot.2021.104596
Jonathas Pereira Graças , Mariana Belloti , Joni Esrom Lima , Lázaro Eustáquio Pereira Peres , Vincent Burlat , Elisabeth Jamet , Victor Alexandre Vitorello

Low pH stress (pH < 5.5) triggers sensitivity responses in roots such as cell death (CD) or arrest in elongation which are detrimental to the development of many plant species. The involvement of the cell wall (CW) with these sensitive responses and their spatiotemporal dynamics in the distinct root zones remains poorly understood. The spatio-temporal analysis of primary roots of Arabidopsis thaliana upon low pH (pH 4.6) revealed that the CD repeatedly started in cells of the transition zone (TZ). Then, CD dynamically moved downward to the meristematic zone (MZ) and upward to the early elongation zone (EZ). The dead cells exhibited coordinated in situ DNA fragmentation, highlighted by the deformity in the nuclei of dead cells and positive reaction for Terminal Deoxynucleotidyl Transferase-mediated dUTP Nick-End Labeling (TUNEL). This DNA fragmentation strongly suggests that the low pH-driven CD occurred through a programmed cell death (PCD) pathway. In addition, a decreased CW stiffness in TZ epidermal cells before the onset of CD suggests that low pH first triggers cell wall disturbances (CWDs) in these root cells. Disruption in CW integrity caused by incorrect cellulose deposition in cobra (cob-1) mutant enhanced CD in TZ and early EZ. Supporting this notion, an increase in calcium concentration upon low pH alleviated the CD in roots, probably due to its role in stabilization of the pectin crosslinking in CWs and likely counteracting the low pH-induced CWDs. Moreover, the CD was significantly decreased when roots were exposed to low pH under reduced CW tension, however, a sudden increase in turgor pressure and CW tension (hypoosmotic treatment) combined with low pH accelerated CD in TZ and early EZ. The CD was not observed in the wild type late EZ trichoblasts upon low pH but rather an orchestrated arrest in elongation. An increase in calcium concentration inhibited this elongation arrest upon low pH, suggesting that the onset of this response also required CWDs. Altogether, these results indicate that low pH-induced CWDs triggered sensitive responses within defined root zones. The low pH-activated PCD and an orchestrated elongation arrest occurring in different root zones suggest the occurrence of yet to be identified signaling cascades.



中文翻译:

拟南芥根中低 pH 值诱导的细胞壁紊乱导致不同根区的模式特异性程序性细胞死亡,并在晚期伸长区阻止伸长

低 pH 胁迫 (pH < 5.5) 会触发根的敏感性反应,例如细胞死亡 (CD) 或伸长停滞,这对许多植物物种的发育有害。细胞壁 (CW) 与这些敏感反应的参与及其在不同根区中的时空动态仍然知之甚少。拟南芥初生根在低 pH 值 (pH 4.6) 下的时空分析表明 CD 在过渡区 (TZ) 的细胞中反复开始。然后,CD 动态向下移动到分生区 (MZ) 并向上移动到早期伸长区 (EZ)。死细胞表现出原位协调DNA 片段化,通过死细胞核的畸形和末端脱氧核苷酸转移酶介导的 dUTP 缺口末端标记 (TUNEL) 的阳性反应来突出显示。这种 DNA 碎片强烈表明低 pH 驱动的 CD 是通过程序性细胞死亡 (PCD) 途径发生的。此外,CD 发作前 TZ 表皮细胞中 CW 刚度的降低表明低 pH 首先触发这些根细胞中的细胞壁紊乱 (CWD)。眼镜蛇( cob-1) 中不正确的纤维素沉积导致 CW 完整性破坏) 突变体增强了 TZ 和早期 EZ 中的 CD。支持这一观点,低 pH 值时钙浓度的增加减轻了根中的 CD,这可能是由于它在稳定 CW 中果胶交联方面的作用,并可能抵消低 pH 值诱导的 CWD。此外,当根在 CW 张力降低的情况下暴露于低 pH 值时,CD 显着降低,然而,膨胀压力和 CW 张力的突然增加(低渗处理)结合低 pH 值加速了 TZ 和早期 EZ 中的 CD。在低 pH 条件下,在野生型晚期 EZ 毛母细胞中未观察到 CD,而是在伸长过程中出现了精心策划的停滞。钙浓度的增加在低 pH 值时抑制了这种伸长停止,表明这种反应的开始也需要 CWD。共,这些结果表明,低 pH 值诱导的 CWD 在确定的根区域内触发了敏感反应。不同根区发生的低 pH 激活 PCD 和精心策划的伸长停滞表明发生了尚未确定的信号级联反应。

更新日期:2021-08-01
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