In the intricate world of plant physiology, the uptake of essential micronutrients is fundamental to growth, development, and survival, especially under challenging environmental conditions. Among these nutrients, boron—a trace element required in minuscule quantities—plays a pivotal role. It contributes critically to the structural integrity of plant cell walls and supports the elongation and differentiation of roots and shoots. Conventionally, boron is absorbed by plants primarily through passive diffusion of boric acid across root cells, a process adequate in boron-rich soils. However, in many agricultural landscapes—particularly arid and boron-deficient soils—this passive mechanism proves insufficient, necessitating active biological systems to maintain boron homeostasis and ensure plant vitality.
Recent groundbreaking research spearheaded by Professor Motoki Tominaga at Waseda University reveals the profound influence of the molecular motor protein myosin XI in the active transport of boron within plants. This research elucidates an essential cellular trafficking mechanism underpinning the precise localization and function of the boric acid channel AtNIP5;1 in Arabidopsis thaliana. The controlled positioning of AtNIP5;1 on the plasma membrane of root epidermal cells is critical for efficient boron uptake directly from the soil solution, yet the mechanisms orchestrating this spatial distribution remained unexplored until now.
Myosins, a well-characterized family of ATP-dependent motor proteins, facilitate intracellular transport by moving along actin filaments. Plant-specific myosin XI isoforms are notably responsible for driving cytoplasmic streaming, orchestrating vesicular traffic, and delivering organelles and proteins to designated cellular compartments. This dynamic intracellular motion optimizes cellular function and response, particularly under developmental and environmental stress conditions. Recognizing this, the investigative team hypothesized that myosin XI might regulate the polar localization of AtNIP5;1, thereby modulating boron acquisition in response to nutrient scarcity.
To empirically test this hypothesis, the researchers employed gene knockout techniques to generate multiple Arabidopsis thaliana mutants deficient in three predominant myosin XI proteins—XI-K, XI-2, and XI-1—known for their essential roles in intracellular motility and cytoplasmic streaming. The double (xi-k xi-2) and triple (xi-k xi-1 xi-2) knockout mutants were subjected to growth trials under varying boron concentrations to ascertain physiological and biochemical consequences of disrupted myosin function.
Remarkably, under boron-sufficient growth media, these mutant plants exhibited negligible phenotypic deviations from wild-type counterparts, signaling compensatory mechanisms or alternate pathways operating under non-limiting nutrient conditions. In stark contrast, exposure to boron-depleted environments precipitated profound developmental impairments. Loss of myosin XI function resulted in stunted root elongation, diminished leaf expansion, and strikingly reduced boron content in aerial tissues. These phenotypical changes quantitatively correlated with boron availability, underscoring the indispensable role of myosin XI-mediated transport under nutrient-limiting stress.
High-resolution confocal microscopy investigations provided compelling visual evidence that the polarized distribution of AtNIP5;1 along the outer plasma membrane domain of root epidermal cells was severely perturbed in the absence of functional myosin XI. Instead of the tight, soil-facing localization observed in wild-type plants, AtNIP5;1 distribution in mutant lines became diffuse, non-polar, or mislocalized to intracellular compartments. Such delocalization of the boric acid transporter rationalizes the reduced boron uptake efficiency and resultant phenotypic detriments observed under boron starvation.
The cellular mechanism underlying this mislocalization was further elucidated by probing the endocytic trafficking pathways responsible for membrane protein recycling and spatial maintenance. Employing fluorescent dye tracers and live-cell imaging, the research team demonstrated that endocytosis—the regulated internalization and recycling or degradation of membrane proteins—was significantly impaired in myosin XI-deficient mutants. The deficiency in endocytic flux indicates that myosin XI facilitates the dynamic remodeling and maintenance of plasma membrane protein domains critical for boron transport.
Interestingly, contrasting with AtNIP5;1, the boron transporter AtBOR1, which localizes to internal cellular membranes and mediates intracellular boron distribution, exhibited minimal sensitivity to myosin XI loss. This suggests a differentiated trafficking dependency amongst boron transporters, where AtNIP5;1 requires myosin XI-driven trafficking for plasma membrane polarization, whereas AtBOR1 may be maintained via alternative pathways.
Additional validation was achieved through pharmacological intervention: chemical inhibitors targeting myosin XI ATPase activity and agents disrupting the actin cytoskeleton similarly induced depolarization of AtNIP5;1 in wild-type plants. This parallel between genetic and chemical inhibition experiments strengthens the conclusion that the mechanistic axis involving myosin XI motility along actin filaments is pivotal for the spatial control of boric acid channels during boron uptake.
This discovery opens promising avenues in agricultural biotechnology, especially considering that boron deficiency remains a global challenge impacting crop productivity on millions of hectares of arid and semi-arid farmland. The conservation of myosin XI function across plant species suggests potential translational applications in major cereals such as rice, wheat, and maize. Engineering enhanced expression or function of myosin XI variants or stabilizing polar localization mechanisms of boron channels like AtNIP5;1 could yield crops better equipped to thrive in nutrient-impoverished soils, thus contributing to food security amid escalating soil degradation globally.
Moreover, the study highlights the intricate coordination between intracellular trafficking machinery and nutrient transport pathways, underscoring the cell biological nuances that orchestrate plant adaptation to environmental fluctuations. Understanding these molecular transport systems provides a foundational framework for breeding strategies and genetic engineering aimed at developing plants with optimized nutrient uptake efficiencies.
Reflecting on the broader significance, Professor Tominaga emphasized the translational potential of these findings: “By uncovering how myosin XI governs the precise positioning of essential nutrient transporters, we are beginning to crack the code of how plants manage resource acquisition at a cellular level. This knowledge paves the way for creating crops resilient to nutrient limitations, a critical need for sustainable agriculture in the face of changing climate and soil fertility conditions.”
Looking forward, future research directions include dissecting the precise molecular interactions between myosin XI motors and their cargo vesicles, identifying potential adaptor proteins involved in AtNIP5;1 trafficking, and investigating the regulation of myosin XI activity under different stress cues. Additionally, expanding studies to agriculturally relevant crops and field conditions will be crucial to translate these molecular insights into practical agronomic benefits.
In sum, this pioneering research elucidates a novel role of myosin XI as a central regulator of boron acquisition, highlighting an elegant cellular strategy plants employ to maintain micronutrient homeostasis through targeted intracellular trafficking and membrane protein localization. As the global agriculture sector grapples with nutrient depletion challenges, such fundamental molecular insights offer a hopeful blueprint for innovation and resilience.
Subject of Research:
Not applicable
Article Title:
Myosin XI is required for boron transport under boron limitation via maintenance of endocytosis and polar localization of the boric acid channel AtNIP5;1
News Publication Date:
17-Apr-2025
Web References:
https://www.sciencedirect.com/science/article/pii/S0981942825004668
http://dx.doi.org/10.1016/j.plaphy.2025.109938
References:
Authors: Haiyang Liu, Keita Muro, Riku Chishima, Junpei Takano, Motoki Tominaga
Image Credits:
Professor Motoki Tominaga, Waseda University, Japan
Keywords:
Plant sciences, Plant anatomy, Plants, Plant physiology, Biochemistry, Plant biochemistry, Cell biology, Agriculture, Crop science, Crop yields
