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Cellular and Molecular Regulatory Signals in Root Growth and Development

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (20 September 2024) | Viewed by 10437

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Prof. Dr. Guzel Kudoyarova

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Laboratory of Plant Physiology, Ufa Institute of Biology of the Russian Academy of Sciences, Ufa 450054, Russia
Interests: plant productivity; phytohormones; plant growth promoting bacteria; bacterial metabolites; plant-microorganism interaction
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Dear Colleagues,

Responses of root growth and development to environmental changes ensure adequate adaptation of plants to availability of water and nutrients. For example, accelerating root elongation allows them to reach deeper soil layers, where water is still stored during drought, when the top layers become dry. Increased root branching in the soil patches enriched with mineral nutrients facilitates their acquisition by plants. These types of responses are initiated by environmental signals that induce and interact with endogenous signals resulting in the changes in division, elongation and differentiation of root cells. Although the complicated net of these signals has been thoroughly studied, many questions still remain unanswered. Therefore we invite researchers to submit their experimental and review articles to the present Special Issue. The articles should address (but not be limited to) the following topics:

sensors of water and nutrients availability (osmosensors and receptors, such as NRT, translating changes in concentration of essential elements into root developmental changes);
control of root growth and development by transcription factors, MAP kinase modules and secondary messengers (PLETHORA, WUSCHEL-related homeobox, MYB, WRKY, NAC and other translation factors; reactive oxygen species, nitric oxide);
hormonal control of root growth and development (root cell division, elongation and differentiation; initiation of lateral root primordia and their emergence; root hair formation; differentiation of secondary walls);
influence of water deficit on local and distant signals controlling root growth and developments;
effects of toxic compounds on root growth and development (such as heavy metals, herbicides, high concentration of sodium and others);
regulatory signals generated by plant growth promoting bacteria and their effects on root growth and development.

Prof. Dr. Guzel Kudoyarova
Guest Editor

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Keywords

reactive oxygen species
water supply and deficit
root apoplastic barriers
root architecture
nutrients uptake

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Published Papers (7 papers)

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Research

30 pages, 5968 KiB

Open AccessArticle

Nitrate Starvation Induces Lateral Root Organogenesis in Triticum aestivum via Auxin Signaling

by Chengming Tang, Yunxiu Zhang, Xiao Liu, Bin Zhang, Jisheng Si, Haiyong Xia, Shoujin Fan and Lingan Kong

Int. J. Mol. Sci. 2024, 25(17), 9566; https://doi.org/10.3390/ijms25179566 - 3 Sep 2024

Viewed by 509

Abstract

The lateral root (LR) is an essential component of the plant root system, performing important functions for nutrient and water uptake in plants and playing a pivotal role in cereal crop productivity. Nitrate (NO₃⁻) is an essential nutrient for plants. In this study, wheat plants were grown in 1/2 strength Hoagland’s solution containing 5 mM NO₃⁻ (check; CK), 0.1 mM NO₃⁻ (low NO₃⁻; LN), or 0.1 mM NO₃⁻ plus 60 mg/L 2,3,5-triiodobenzoic acid (TIBA) (LNT). The results showed that LN increased the LR number significantly at 48 h after treatment compared with CK, while not increasing the root biomass, and LNT significantly decreased the LR number and root biomass. The transcriptomic analysis showed that LN induced the expression of genes related to root IAA synthesis and transport and cell wall remodeling, and it was suppressed in the LNT conditions. A physiological assay revealed that the LN conditions increased the activity of IAA biosynthesis-related enzymes, the concentrations of tryptophan and IAA, and the activity of cell wall remodeling enzymes in the roots, whereas the content of polysaccharides in the LRP cell wall was significantly decreased compared with the control. Fourier-transform infrared spectroscopy and atomic microscopy revealed that the content of cell wall polysaccharides decreased and the cell wall elasticity of LR primordia (LRP) increased under the LN conditions. The effects of LN on IAA synthesis and polar transport, cell wall remodeling, and LR development were abolished when TIBA was applied. Our findings indicate that NO₃⁻ starvation may improve auxin homeostasis and the biological properties of the LRP cell wall and thus promote LR initiation, while TIBA addition dampens the effects of LN on auxin signaling, gene expression, physiological processes, and the root architecture. Full article

(This article belongs to the Special Issue Cellular and Molecular Regulatory Signals in Root Growth and Development)

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15 pages, 20220 KiB

Open AccessArticle

MicroRNAs Participate in Morphological Acclimation of Sugar Beet Roots to Nitrogen Deficiency

by Xinyu Liu, Zhenqiang Lu, Qi Yao, Lingqing Xu, Jingjing Fu, Xilong Yin, Qing Bai, Dali Liu and Wang Xing

Int. J. Mol. Sci. 2024, 25(16), 9027; https://doi.org/10.3390/ijms25169027 - 20 Aug 2024

Viewed by 405

Abstract

Nitrogen (N) is essential for sugar beet (Beta vulgaris L.), a highly N-demanding sugar crop. This study investigated the morphological, subcellular, and microRNA-regulated responses of sugar beet roots to low N (LN) stress (0.5 mmol/L N) to better understand the N perception, uptake, and utilization in this species. The results showed that LN led to decreased dry weight of roots, N accumulation, and N dry matter production efficiency, along with damage to cell walls and membranes and a reduction in organelle numbers (particularly mitochondria). Meanwhile, there was an increase in root length (7.2%) and branch numbers (29.2%) and a decrease in root surface area (6.14%) and root volume (6.23%) in sugar beet after 7 d of LN exposure compared to the control (5 mmol/L N). Transcriptomics analysis was confirmed by qRT-PCR for 6 randomly selected microRNAs, and we identified 22 differentially expressed microRNAs (DEMs) in beet root under LN treatment. They were primarily enriched in functions related to binding (1125), ion binding (641), intracellular (437) and intracellular parts (428), and organelles (350) and associated with starch and sucrose metabolism, tyrosine metabolism, pyrimidine metabolism, amino sugar and nucleotide sugar metabolism, and isoquinoline alkaloid biosynthesis, as indicated by the GO and KEGG analyses. Among them, the upregulated miR156a, with conserved sequences, was identified as a key DEM that potentially targets and regulates squamosa promoter-binding-like proteins (SPLs, 104889216 and 104897537) through the microRNA-mRNA network. Overexpression of miR156a (MIR) promoted root growth in transgenic Arabidopsis, increasing the length, surface area, and volume. In contrast, silencing miR156a (STTM) had the opposite effect. Notably, the fresh root weight decreased by 45.6% in STTM lines, while it increased by 27.4% in MIR lines, compared to the wild type (WT). It can be inferred that microRNAs, especially miR156, play crucial roles in sugar beet root’s development and acclimation to LN conditions. They likely facilitate active responses to N deficiency through network regulation, enabling beet roots to take up nutrients from the environment and sustain their vital life processes. Full article

(This article belongs to the Special Issue Cellular and Molecular Regulatory Signals in Root Growth and Development)

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20 pages, 5039 KiB

Open AccessArticle

Knockdown of microRNA390 Enhances Maize Brace Root Growth

by Juan Meng, Weiya Li, Feiyan Qi, Tianxiao Yang, Na Li, Jiong Wan, Xiaoqi Li, Yajuan Jiang, Chenhui Wang, Meilian Huang, Yuanyuan Zhang, Yongqiang Chen, Sachin Teotia, Guiliang Tang, Zhanhui Zhang and Jihua Tang

Int. J. Mol. Sci. 2024, 25(12), 6791; https://doi.org/10.3390/ijms25126791 - 20 Jun 2024

Viewed by 3652

Abstract

Brace root architecture is a critical determinant of maize’s stalk anchorage and nutrition uptake, influencing root lodging resistance, stress tolerance, and plant growth. To identify the key microRNAs (miRNAs) in control of maize brace root growth, we performed small RNA sequencing using brace root samples at emergence and growth stages. We focused on the genetic modulation of brace root development in maize through manipulation of miR390 and its downstream regulated auxin response factors (ARFs). In the present study, miR167, miR166, miR172, and miR390 were identified to be involved in maize brace root growth in inbred line B73. Utilizing short tandem target mimic (STTM) technology, we further developed maize lines with reduced miR390 expression and analyzed their root architecture compared to wild-type controls. Our findings show that STTM390 maize lines exhibit enhanced brace root length and increased whorl numbers. Gene expression analyses revealed that the suppression of miR390 leads to upregulation of its downstream regulated ARF genes, specifically ZmARF11 and ZmARF26, which may significantly alter root architecture. Additionally, loss-of-function mutants for ZmARF11 and ZmARF26 were characterized to further confirm the role of these genes in brace root growth. These results demonstrate that miR390, ZmARF11, and ZmARF26 play crucial roles in regulating maize brace root growth; the involved complicated molecular mechanisms need to be further explored. This study provides a genetic basis for breeding maize varieties with improved lodging resistance and adaptability to diverse agricultural environments. Full article

(This article belongs to the Special Issue Cellular and Molecular Regulatory Signals in Root Growth and Development)

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20 pages, 3530 KiB

Open AccessArticle

Whole-Genome Sequencing and Analysis of Tumour-Forming Radish (Raphanus sativus L.) Line

by Xenia Kuznetsova, Irina Dodueva, Alexey Afonin, Emma Gribchenko, Lavrentii Danilov, Maria Gancheva, Varvara Tvorogova, Nikita Galynin and Lyudmila Lutova

Int. J. Mol. Sci. 2024, 25(11), 6236; https://doi.org/10.3390/ijms25116236 - 5 Jun 2024

Viewed by 692

Abstract

Spontaneous tumour formation in higher plants can occur in the absence of pathogen invasion, depending on the plant genotype. Spontaneous tumour formation on the taproots is consistently observed in certain inbred lines of radish (Raphanus sativus var. radicula Pers.). In this paper, using Oxford Nanopore and Illumina technologies, we have sequenced the genomes of two closely related radish inbred lines that differ in their ability to spontaneously form tumours. We identified a large number of single nucleotide variants (amino acid substitutions, insertions or deletions, SNVs) that are likely to be associated with the spontaneous tumour formation. Among the genes involved in the trait, we have identified those that regulate the cell cycle, meristem activity, gene expression, and metabolism and signalling of phytohormones. After identifying the SNVs, we performed Sanger sequencing of amplicons corresponding to SNV-containing regions to validate our results. We then checked for the presence of SNVs in other tumour lines of the radish genetic collection and found the ERF118 gene, which had the SNVs in the majority of tumour lines. Furthermore, we performed the identification of the CLAVATA3/ESR (CLE) and WUSCHEL (WOX) genes and, as a result, identified two unique radish CLE genes which probably encode proteins with multiple CLE domains. The results obtained provide a basis for investigating the mechanisms of plant tumour formation and also for future genetic and genomic studies of radish. Full article

(This article belongs to the Special Issue Cellular and Molecular Regulatory Signals in Root Growth and Development)

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23 pages, 18479 KiB

Open AccessArticle

Do DEEPER ROOTING 1 Homologs Regulate the Lateral Root Slope Angle in Cucumber (Cucumis sativus)?

by Alexey S. Kiryushkin, Elena L. Ilina, Tatyana Y. Kiikova, Katharina Pawlowski and Kirill N. Demchenko

Int. J. Mol. Sci. 2024, 25(4), 1975; https://doi.org/10.3390/ijms25041975 - 6 Feb 2024

Cited by 1 | Viewed by 1381

Abstract

The architecture of the root system is fundamental to plant productivity. The rate of root growth, the density of lateral roots, and the spatial structure of lateral and adventitious roots determine the developmental plasticity of the root system in response to changes in environmental conditions. One of the genes involved in the regulation of the slope angle of lateral roots is DEEPER ROOTING 1 (DRO1). Its orthologs and paralogs have been identified in rice, Arabidopsis, and several other species. However, nothing is known about the formation of the slope angle of lateral roots in species with the initiation of lateral root primordia within the parental root meristem. To address this knowledge gap, we identified orthologs and paralogs of the DRO1 gene in cucumber (Cucumis sativus) using a phylogenetic analysis of IGT protein family members. Differences in the transcriptional response of CsDRO1, CsDRO1-LIKE1 (CsDRO1L1), and CsDRO1-LIKE2 (CsDRO1L2) to exogenous auxin were analyzed. The results showed that only CsDRO1L1 is auxin-responsive. An analysis of promoter–reporter fusions demonstrated that the CsDRO1, CsDRO1L1, and CsDRO1L2 genes were expressed in the meristem in cell files of the central cylinder, endodermis, and cortex; the three genes displayed different expression patterns in cucumber roots with only partial overlap. A knockout of individual CsDRO1, CsDRO1L1, and CsDRO1L2 genes was performed via CRISPR/Cas9 gene editing. Our study suggests that the knockout of individual genes does not affect the slope angle formation during lateral root primordia development in the cucumber parental root. Full article

(This article belongs to the Special Issue Cellular and Molecular Regulatory Signals in Root Growth and Development)

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22 pages, 6671 KiB

Open AccessArticle

Nutrient Solution Flowing Environment Affects Metabolite Synthesis Inducing Root Thigmomorphogenesis of Lettuce (Lactuca sativa L.) in Hydroponics

by Bateer Baiyin, Yue Xiang, Jiangtao Hu, Kotaro Tagawa, Jung Eek Son, Satoshi Yamada and Qichang Yang

Int. J. Mol. Sci. 2023, 24(23), 16616; https://doi.org/10.3390/ijms242316616 - 22 Nov 2023

Cited by 5 | Viewed by 1480

Abstract

The principal difference between hydroponics and other substrate cultivation methods is the flowing liquid hydroponic cultivation substrate. Our previous studies have revealed that a suitable flowing environment of nutrient solution promoted root development and plant growth, while an excess flow environment was unfavorable for plants. To explain the thigmomorphogenetic response of excess flow-induced metabolic changes, six groups of lettuce (Lactuca sativa L.), including two flow conditions and three time periods, were grown. Compared with the plants without flow, the plants with flow showed decreased root fresh weight, total root length, root surface area, and root volume but increased average root diameter and root density. The roots with flow had more upregulated metabolites than those without flow, suggesting that the flow may trigger metabolic synthesis and activity. Seventy-nine common differential metabolites among six groups were screened, and enrichment analysis showed the most significant enrichment in the arginine biosynthesis pathway. Arginine was present in all the groups and exhibited greater concentrations in roots with flow than without flow. It can be speculated from the results that a high-flowing environment of nutrient solution promotes arginine synthesis, resulting in changes in root morphology. The findings provide insights on root thigmomorphogenesis affected by its growing conditions and help understand how plants respond to environmental mechanical forces. Full article

(This article belongs to the Special Issue Cellular and Molecular Regulatory Signals in Root Growth and Development)

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13 pages, 6271 KiB

Open AccessArticle

Immunolocalization of Jasmonates and Auxins in Pea Roots in Connection with Inhibition of Root Growth under Salinity Conditions

by Guzel Akhiyarova, Gyulnar Vafina, Dmitriy Veselov and Guzel Kudoyarova

Int. J. Mol. Sci. 2023, 24(20), 15148; https://doi.org/10.3390/ijms242015148 - 13 Oct 2023

Cited by 2 | Viewed by 1182

Abstract

Inhibition of root elongation is an important growth response to salinity, which is thought to be regulated by the accumulation of jasmonates and auxins in roots. Nevertheless, the mechanisms of the interaction of these hormones in the regulation of the growth response to salinity are still not clear enough. Their better understanding depends on the study of the distribution of jasmonates and auxins between root cells. This was achieved with the help of immunolocalization of auxin (indoleacetic acid) and jasmonates on the root sections of pea plants. Salinity inhibited root elongation and decreased the size of the meristem zone and the length of cells in the elongation zone. Immunofluorescence based on the use of appropriate, specific antibodies that recognize auxins and jasmonates revealed an increased abundance of both hormones in the meristem zone. The obtained data suggests the participation of either auxins or jasmonates in the inhibition of cell division, which leads to a decrease in the size of the meristem zone. The level of only auxin and not jasmonate increased in the elongation zone. However, since some literature evidence argues against inhibition of root cell division by auxins, while jasmonates have been shown to inhibit this process, we came to the conclusion that elevated jasmonate is a more likely candidate for inhibiting root meristem activity under salinity conditions. Data suggests that auxins, not jasmonates, reduce cell size in the elongation zone of salt-stressed plants, a suggestion supported by the known ability of auxins to inhibit root cell elongation. Full article

(This article belongs to the Special Issue Cellular and Molecular Regulatory Signals in Root Growth and Development)

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