Bundling up the Role of the Actin Cytoskeleton in Primary Root Growth

Abstract

Primary root growth is required by the plant to anchor in the soil and reach out for nutrients and water, while dealing with obstacles. Efficient root elongation and bending depends upon the coordinated action of environmental sensing, signal transduction, and growth responses. The actin cytoskeleton is a highly plastic network that constitutes a point of integration for environmental stimuli and hormonal pathways. In this review, we present a detailed compilation highlighting the importance of the actin cytoskeleton during primary root growth and we describe how actin-binding proteins, plant hormones, and actin-disrupting drugs affect root growth and root actin. We also discuss the feedback loop between actin and root responses to light and gravity. Actin affects cell division and elongation through the control of its own organization. We remark upon the importance of longitudinally oriented actin bundles as a hallmark of cell elongation as well as the role of the actin cytoskeleton in protein trafficking and vacuolar reshaping during this process. The actin network is shaped by a plethora of actin-binding proteins; however, there is still a large gap in connecting the molecular function of these proteins with their developmental effects. Here, we summarize their function and known effects on primary root growth with a focus on their high level of specialization. Light and gravity are key factors that help us understand root growth directionality. The response of the root to gravity relies on hormonal, particularly auxin, homeostasis, and the actin cytoskeleton. Actin is necessary for the perception of the gravity stimulus via the repositioning of sedimenting statoliths, but it is also involved in mediating the growth response via the trafficking of auxin transporters and cell elongation. Furthermore, auxin and auxin analogs can affect the composition of the actin network, indicating a potential feedback loop. Light, in its turn, affects actin organization and hence, root growth, although its precise role remains largely unknown. Recently, fundamental studies with the latest techniques have given us more in-depth knowledge of the role and organization of actin in the coordination of root growth; however, there remains a lot to discover, especially in how actin organization helps cell shaping, and therefore root growth.

Quantitative trait loci mapping reveals important genomic regions controlling root architecture and shoot biomass under nitrogen, phosphorus, and potassium stress in rapeseed (Brassica napus L.)

“…Similarly, some important candidate genes were identified in the major QTL cluster qcC06-1 . For example, a gene ( BnaC06g12200D, AtVLN4) has been detected at a distance of 102 Kb from the peak position and reported to regulate root growth and development under different abiotic stresses ( García-González and van Gelderen, 2021 ). These potential candidate genes were found in strong interaction with other genes in the protein interaction network ( Figure 5B ).…”

Protein interactome of 3′,5′‐cAMP reveals its role in regulating the actin cytoskeleton

“…An increase of the 3′,5′‐cAMP levels was sufficient to complement the act2act7 short hypocotyl phenotype, arguing for the role of 3′,5′‐cAMP in the regulation of actin cytoskeleton possibly by inducing actin bundling, as observed in the 3′,5′‐cAMP‐treated 35S:GFP‐FABD seedlings. However, it should be noted that the 3′,5′‐cAMP treatment did not affect the hypocotyl length of the WT plants, and the interplay between actin bundling and cell expansion is also not fully understood (Garcia‐Gonzalez & van Gelderen, 2021). The role of 3′,5′‐cAMP, and PKA signaling in the dynamics of the actin cytoskeleton was reported in animal cells (Gerits et al., 2007), such as in the context of actin‐dependent cell migration (Howe, 2004) and neuronal growth (Chen et al., 2003).…”

Dynamic Dark Root Chamber: Advancing non-invasive phenotyping of roots kept in darkness using infrared imaging

“…One of the most important environmental factors that plants perceive and respond to is light. Different wavelengths of light spectrum can provide energy for photosynthesis, or act as a signal that informs plants about the quality of the light source (Miotto et al ., 2021; van Gelderen et al ., 2021). Plants express various photoreceptors that sense different wavelengths of light and accordingly trigger specific responses in the shoot, but also in the root (Van Gelderen, Kang and Pierik, 2018; Retzer and Weckwerth, 2021, 2023; Lopez et al ., 2023).…”

“…Root meristem activity, which determines the root growth potential, decreases when roots are exposed to light, while the elongation rate, which determines the root length, increases and directional growth deviates more from vertical upon direct root illumination (Mo et al ., 2015; Silva-Navas et al ., 2016; Shi et al ., 2018; Lacek et al ., 2021). These changes in root growth are accompanied by changes in cell morphology, such as altered cell size, as well as altered cytoskeleton arrangement, which are well described processes that steer root growth modulation (Dyachok et al ., 2011; Silva-Navas et al ., 2016; Halat, Gyte and Wasteneys, 2020; García-González and van Gelderen, 2021). Light stress also affects the hormonal balance and responses in the root.…”