HY5 regulates light‐responsive transcription of microRNA163 to promote primary root elongation in Arabidopsis seedlings

Abstract

MicroRNAs (miRNAs) play key roles in the posttranscriptional regulation of gene expression in plants. Many miRNAs are responsive to environmental signals. Light is the first environmental signal perceived by plants after emergence from the soil. However, less is known about the roles and regulatory mechanism of miRNAs in response to light signal. Here, using small RNA sequencing, we determined that miR163 is significantly rapidly induced by light signaling in Arabidopsis thaliana seedlings. The light-inducible response of miR163 functions genetically downstream of LONG HYPO-COTYL 5 (HY5), a central positive regulator of photomorphogenesis. HY5 directly binds to the two G/Chybrid elements in the miR163 promoter with unequal affinity; one of these elements, which is located next to the transcription start site, plays a major role in light-induced expression of miR163. Overexpression of miR163 rescued the defective primary root elongation of hy5 seedlings without affecting lateral root growth, whereas overexpressing of miR163 target PXMT1 inhibited primary root elongation. These findings provide insight into understanding the post-transcriptional regulation of root photomorphogenesis mediated by the HY5-miR163-PXMT1 network.

In Arabidopsis thaliana, RNA-Induced Silencing Complex-Loading of MicroRNAs Plays a Minor Regulatory Role During Photomorphogenesis Except for miR163

“…miRNA163 was exceptional, it accumulated to low levels in the D input, while it was dramatically increased (∼20.5-fold) in the L input ( Supplementary Table 2A ). These results are consistent with previous results showing that during photomorphogenesis, miRNA163 was dramatically upregulated, while the expression of other miRNAs was changed slightly ( Choi et al, 2020 ; Li et al, 2021 ).…”

“…First, we compared the miRNAome of D and L inputs. In line with previous studies ( Choi et al, 2020 ; Li et al, 2021 ), we found that the miRNAomes of D and L inputs were moderately different and 10/34 miRNAs accumulated significantly different ( Figure 2 and Supplementary Table 2A ). However, the changes are modest, only four miRNAs (miR163, miR319a, miR408, and miR482) showed more than 2-fold differences.…”

“…Previous studies reported conflicting results about the role of miRNAs in the regulation of photomorphogenesis. While findings that miRNA biogenesis factors and certain miRNAs are required for normal photomorphogenesis and that miRNA-guided RISC cleavage activity is increased during de-etiolation indicate that miRNA regulation plays an important role in the control of photomorphogenesis, and the results that the total miRNAome is only slightly changed during de-etiolation suggest that miRNAs do not play a critical regulatory role ( Choi et al, 2020 ; Li et al, 2021 ). These studies compared total miRNAomes during de-etiolation supposing that it represents the functional miRNAome.…”

HY5: A Pivotal Regulator of Light-Dependent Development in Higher Plants

“…HY5 decreases the abundance of auxin transporters PIN-FORMED3 and LIKE-AUX1 3 in the plasma membrane to inhibit lateral growth under low red:far-red light conditions ( van Gelderen et al, 2018 ). Red and blue lights stabilize the HY5 dependent on phyB or CRYs in the root, where it activates the miR163 and itself to promote primary root growth ( Gao et al, 2021 ; Li T. et al, 2021 ). Thus, these results suggest that distinct wavelength-specific photoreceptors transduce the light signals to HY5 in the root cells where it regulates the root growth in the soil.…”

Differential Responses of Wheat (Triticum aestivum L.) and Cotton (Gossypium hirsutum L.) to Nitrogen Deficiency in the Root Morpho-Physiological Characteristics and Potential MicroRNA-Mediated Mechanisms

“…Studies also show that miRNAs regulated root growth and development ( Meng et al, 2010 ; Khan et al, 2011 ; Li and Zhang, 2016 ), including embryonic root development, primary root growth, root radial patterning, tissue differentiation, lateral root, and adventitious root development. By targeting PXMT1, overexpression of miR163 inhibited primary root elongation ( Li T. et al, 2021 ). miR393 with a si-TAAR suppressed primary root elongation which was involved in the abscisic acid (ABA) signaling pathway ( Chen et al, 2012 ; Yan et al, 2022 ); miR393 suppressed root growth by targeting AFB3 in Arabidopsis ( Vidal et al, 2010 ).…”