Boron supply restores aluminum‐blocked auxin transport by the modulation of PIN2 trafficking in the root apical transition zone. (23rd February 2023)

• Record Type: Journal Article
• Authors: Tao, Lin; Xiao, Xiaoyi; Huang, Qiuyu; Zhu, Hu; Feng, Yingming; Li, Yalin; Li, Xuewen; Guo, Zhishan; Liu, Jiayou; Wu, Feihua; Pirayesh, Niloufar; Mahmud, Sakil; Shen, Ren Fang; Shabala, Sergey; Baluška, František; Shi, Lei; Yu, Min
• Is Part Of: Plant journal. Volume 114:Number 1(2023)
• Page Start: 176
• Page End: 192
• Publication Date: 2023-02-23
• Subjects: aluminum toxicity -- endocytosis -- polar auxin transport -- root meristem -- elongation zone; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.16129
• Languages: English
• ISSNs: 0960-7412

Abstract

SUMMARY: The supply of boron (B) alleviates the toxic effects of aluminum (Al) on root growth; however, the mechanistic basis of this process remains elusive. This study filled this knowledge gap, demonstrating that boron modifies auxin distribution and transport in Al‐exposed Arabidopsis roots. In B‐deprived roots, treatment with Al induced an increase in auxin content in the root apical meristem zone (MZ) and transition zone (TZ), whereas in the elongation zone (EZ) the auxin content was decreased beyond the level required for adequate growth. These distribution patterns are explained by the fact that basipetal auxin transport from the TZ to the EZ was disrupted by Al‐inhibited PIN‐FORMED 2 (PIN2) endocytosis. Experiments involving the modulation of protein biosynthesis by cycloheximide (CHX) and transcriptional regulation by cordycepin (COR) demonstrated that the Al‐induced increase of PIN2 membrane proteins was dependent upon the inhibition of PIN2 endocytosis, rather than on the transcriptional regulation of the PIN2 gene. Experiments reporting on the profiling of Al 3+ and PIN2 proteins revealed that the inhibition of endocytosis of PIN2 proteins was the result of Al‐induced limitation of the fluidity of the plasma membrane. The supply of B mediated the turnover of PIN2 endosomes conjugated with indole‐3‐acetic acid (IAA), and thus restored the Al‐induced inhibition of IAA transport through the TZ to the EZ. Overall, the reported results demonstrate that boron supply mediates PIN2 endosome‐based auxin transport to alleviate Al toxicity in plant roots. Significance Statement: Aluminum toxicity and boron deficiency are limiting factors for agricultural production in acid soils, which make up almost half of the world's arable land. Boron fertilization alleviates aluminum toxicity but the mechanism remains unclear. The study shows that boron supply releases aluminum‐induced root growth arrest by facilitating endosome‐based polar auxin transport via PIN2 polar localization in the upper half of the plasma membrane (shootward). We provide solid support for boron fertilizer in remediating aluminum toxicity in acid soils.