Disruption of CYCLOPHILIN 38 function reveals a photosynthesis-dependent systemic signal controlling lateral root emergence

AbstractPhotosynthesis in leaves generates the fixed-carbon resources and essential metabolites that support sink tissues, such as roots [1]. One of these products, sucrose, is known to promote primary root growth, but it is not clear what other molecules may be involved and whether other stages of root system development are affected by photosynthate levels [2]. Through a mutant screen to identify pathways regulating root system architecture, we identified a mutation in the CYCLOPHILIN 38 (CYP38) gene, which causes an accumulation of pre-emergent stage lateral roots, with a minor effect on primary root growth. CYP38 was previously reported to maintain the stability of Photosystem II (PSII) in chloroplasts [3]. CYP38 expression is enriched in the shoot and grafting experiments show that the gene acts non-cell autonomously to promote lateral root emergence. Growth of wild-type plants under low light conditions phenocopied the cyp38 lateral root emergence phenotype as did the inhibition of PSII-dependent electron transport or NADPH production. Importantly, the cyp38 root phenotype is not rescued by exogenous sucrose, suggesting the involvement of another metabolite. Auxin (IAA) is an essential hormone promoting root growth and its biosynthesis from tryptophan is dependent on reductant generated during photosynthesis [4,5]. Both WT seedlings grown under low light and cyp38 mutants have highly diminished levels of IAA in root tissues. The cyp38 lateral root defect is rescued by IAA treatment, revealing that photosynthesis promotes lateral root emergence partly through IAA biosynthesis. Metabolomic profiling shows that the accumulation of several defense-related metabolites are also photosynthesis-dependent, suggesting that the regulation of a number of energy-intensive pathways are down-regulated when light becomes limiting.

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AT-HOOK MOTIF NUCLEAR LOCALISED PROTEIN 18 as a Novel Modulator of Root System Architecture

10.20944/preprints202003.0046.v1 ◽

2020 ◽

Author(s):

Marek Šírl ◽

Tereza Šnajdrová ◽

Dolores Gutiérrez-Alanís ◽

Joseph G. Dubrovsky ◽

Jean Phillipe Vielle-Calzada ◽

...

Keyword(s):

Root System ◽

System Architecture ◽

Lateral Root ◽

Apical Meristem ◽

Lateral Roots ◽

Primary Root ◽

Root System Architecture ◽

Root Apical Meristem ◽

Root Initiation ◽

Lateral Root Initiation

The AT-HOOK MOTIF NUCLEAR LOCALIZED PROTEIN (AHL) gene family encodes embryophyte-specific nuclear proteins with DNA binding activity. They modulate gene expression and affect various developmental processes in plants. We identify AHL18 (At3G60870) as a developmental modulator of root system architecture and growth. AHL18 regulates the length of the proliferation domain and number of dividing cells in the root apical meristem and thereby, cell production. Both primary root growth and lateral root development respond according to AHL18 transcription level. The ahl18 knock-out plants show reduced root systems due to a shorter primary root and a lower number of lateral roots. This change results from a higher number of arrested and non-developing lateral root primordia (LRP) rather than from decreased initiation. Overexpression of AHL18 results in a more extensive root system, longer primary roots, and increased density of lateral root initiation events. Formation of lateral roots is affected during the initiation of LRP and later development. AHL18 regulate root apical meristem activity, lateral root initiation and emergence, which is in accord with localization of its expression.

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Same same, but different: growth responses of primary and lateral roots

Journal of Experimental Botany ◽

10.1093/jxb/eraa027 ◽

2020 ◽

Vol 71 (8) ◽

pp. 2397-2411 ◽

Cited By ~ 9

Author(s):

Sascha Waidmann ◽

Elizabeth Sarkel ◽

Jürgen Kleine-Vehn

Keyword(s):

Root System ◽

Lateral Root ◽

Growth Regulation ◽

Lateral Roots ◽

Primary Root ◽

Spatial Arrangement ◽

Root System Architecture ◽

Growth Responses ◽

Lateral Root Primordia ◽

Organ Growth

Abstract The root system architecture describes the shape and spatial arrangement of roots within the soil. Its spatial distribution depends on growth and branching rates as well as directional organ growth. The embryonic primary root gives rise to lateral (secondary) roots, and the ratio of both root types changes over the life span of a plant. Most studies have focused on the growth of primary roots and the development of lateral root primordia. Comparably less is known about the growth regulation of secondary root organs. Here, we review similarities and differences between primary and lateral root organ growth, and emphasize particularly how external stimuli and internal signals differentially integrate root system growth.

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Bacillus megaterium Rhizobacteria Promote Growth and Alter Root-System Architecture Through an Auxin- and Ethylene-Independent Signaling Mechanism in Arabidopsis thaliana

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-20-2-0207 ◽

2007 ◽

Vol 20 (2) ◽

pp. 207-217 ◽

Cited By ~ 146

Author(s):

José López-Bucio ◽

Juan Carlos Campos-Cuevas ◽

Erasto Hernández-Calderón ◽

Crisanto Velásquez-Becerra ◽

Rodolfo Farías-Rodríguez ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Root Growth ◽

Root Hair ◽

Lateral Root ◽

Root Formation ◽

Growth Promotion ◽

Primary Root ◽

Root System Architecture ◽

Ethylene Signaling ◽

Primary Root Growth

Soil microorganisms are critical players in plant-soil interactions at the rhizosphere. We have identified a Bacillus megaterium strain that promoted growth and development of bean (Phaseolus vulgaris) and Arabidopsis thaliana plants. We used Arabidopsis thaliana as a model to characterize the effects of inoculation with B. megaterium on plant-growth promotion and postembryonic root development. B. megaterium inoculation caused an inhibition in primary-root growth followed by an increase in lateral-root number, lateral-root growth, and root-hair length. Detailed cellular analyses revealed that primary root-growth inhibition was caused both by a reduction in cell elongation and by reduction of cell proliferation in the root meristem. To study the contribution of auxin and ethylene signaling pathways in the alterations in root-system architecture elicited by B. megaterium, a suite of plant hormone mutants of Arabidopsis, including aux1-7, axr4-1, eir1, etr1, ein2, and rhd6, defective in either auxin or ethylene signaling, were evaluated for their responses to inoculation with this bacteria. When inoculated, all mutant lines tested showed increased biomass production. Moreover, aux1-7 and eir1, which sustain limited root-hair and lateral-root formation when grown in uninoculated medium, were found to increase the number of lateral roots and to develop long root hairs when inoculated with B. megaterium. The ethylene-signaling mutants etr1 and ein2 showed an induction in lateral-root formation and root-hair growth in response to bacterial inoculation. Taken together, our results suggest that plant-growth promotion and root-architectural alterations by B. megaterium may involve auxin- and-ethylene independent mechanisms.

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At-Hook Motif Nuclear Localised Protein 18 as a Novel Modulator of Root System Architecture

International Journal of Molecular Sciences ◽

10.3390/ijms21051886 ◽

2020 ◽

Vol 21 (5) ◽

pp. 1886 ◽

Cited By ~ 3

Author(s):

Marek Širl ◽

Tereza Šnajdrová ◽

Dolores Gutiérrez-Alanís ◽

Joseph G. Dubrovsky ◽

Jean Phillipe Vielle-Calzada ◽

...

Keyword(s):

Root System ◽

System Architecture ◽

Lateral Root ◽

Apical Meristem ◽

Lateral Roots ◽

Primary Root ◽

Root System Architecture ◽

Root Apical Meristem ◽

Root Initiation ◽

Lateral Root Initiation

The At-Hook Motif Nuclear Localized Protein (AHL) gene family encodes embryophyte-specific nuclear proteins with DNA binding activity. They modulate gene expression and affect various developmental processes in plants. We identify AHL18 (At3G60870) as a developmental modulator of root system architecture and growth. AHL18 is involved in regulation of the length of the proliferation domain and number of dividing cells in the root apical meristem and thereby, cell production. Both primary root growth and lateral root development respond according to AHL18 transcription level. The ahl18 knock-out plants show reduced root systems due to a shorter primary root and a lower number of lateral roots. This change results from a higher number of arrested and non-developing lateral root primordia (LRP) rather than from a decreased LRP initiation. The over-expression of AHL18 results in a more extensive root system, longer primary roots, and increased density of lateral root initiation events. AHL18 is thus involved in the formation of lateral roots at both LRP initiation and their later development. We conclude that AHL18 participates in modulation of root system architecture through regulation of root apical meristem activity, lateral root initiation and emergence; these correspond well with expression pattern of AHL18.

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Longleaf Pine Root System Development and Seedling Quality in Response to Copper Root Pruning and Cavity Size

Southern Journal of Applied Forestry ◽

10.1093/sjaf/35.1.5 ◽

2011 ◽

Vol 35 (1) ◽

pp. 5-11 ◽

Cited By ~ 8

Author(s):

Mary Anne Sword Sayer ◽

Shi-Jean Susana Sung ◽

James D. Haywood

Keyword(s):

Root Growth ◽

Root System ◽

System Development ◽

Longleaf Pine ◽

Lateral Roots ◽

Dry Weight ◽

Root Pruning ◽

Cavity Size ◽

Root System Development ◽

Primary Lateral

Abstract Cultural practices that modify root system structure in the plug of container-grown seedlings have the potential to improve root system function after planting. Our objective was to assess how copper root pruning affects the quality and root system development of longleaf pine seedlings grown in three cavity sizes in a greenhouse. Copper root pruning increased seedling size, the allocation of root system dry weight to the taproot, and the fraction of fibrous root mass allocated to secondary lateral roots compared with primary lateral roots. It decreased the allocation of root system dry weight to primary lateral roots and led to a distribution of root growth potential that more closely resembled the root growth of naturally sown seedlings. These effects of copper root pruning may benefit longleaf pine establishment. However, because copper root pruning increased competition for cavity growing space among the taproot and fibrous roots, we suggest that recommendations regarding cavity size and seedling quality parameters be tailored for copper-coated cavities.

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Early development and gravitropic response of lateral roots in Arabidopsis thaliana

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2011.0231 ◽

2012 ◽

Vol 367 (1595) ◽

pp. 1509-1516 ◽

Cited By ~ 30

Author(s):

S. Guyomarc'h ◽

S. Léran ◽

M. Auzon-Cape ◽

F. Perrine-Walker ◽

M. Lucas ◽

...

Keyword(s):

Lateral Root ◽

Developmental Plasticity ◽

Lateral Roots ◽

Expression Patterns ◽

Primary Root ◽

Root System Architecture ◽

Specific Response ◽

Root Induction ◽

Root Gravitropism ◽

Auxin Transporter

Root system architecture plays an important role in determining nutrient and water acquisition and is modulated by endogenous and environmental factors, resulting in considerable developmental plasticity. The orientation of primary root growth in response to gravity (gravitropism) has been studied extensively, but little is known about the behaviour of lateral roots in response to this signal. Here, we analysed the response of lateral roots to gravity and, consistently with previous observations, we showed that gravitropism was acquired slowly after emergence. Using a lateral root induction system, we studied the kinetics for the appearance of statoliths, phloem connections and auxin transporter gene expression patterns. We found that statoliths could not be detected until 1 day after emergence, whereas the gravitropic curvature of the lateral root started earlier. Auxin transporters modulate auxin distribution in primary root gravitropism. We found differences regarding PIN3 and AUX1 expression patterns between the lateral root and the primary root apices. Especially PIN3, which is involved in primary root gravitropism, was not expressed in the lateral root columella. Our work revealed new developmental transitions occurring in lateral roots after emergence, and auxin transporter expression patterns that might explain the specific response of lateral roots to gravity.

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The effects of temperature on primary root growth dynamics and lateral root distribution in garden pea (Pisum sativum L., cv. “Alaska”)

Environmental and Experimental Botany ◽

10.1016/0098-8472(93)90070-v ◽

1993 ◽

Vol 33 (2) ◽

pp. 243-258 ◽

Cited By ~ 31

Author(s):

Daniel K. Gladish ◽

Thomas L. Rost

Keyword(s):

Pisum Sativum ◽

Root Growth ◽

Root Distribution ◽

Lateral Root ◽

Primary Root ◽

Growth Dynamics ◽

Garden Pea ◽

Pisum Sativum L ◽

Primary Root Growth ◽

Effects Of Temperature

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Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots

10.1101/572941 ◽

2019 ◽

Author(s):

Sascha Waidmann ◽

Michel Ruiz Rosquete ◽

Maria Schöller ◽

Heike Lindner ◽

Therese LaRue ◽

...

Keyword(s):

Root System ◽

Lateral Root ◽

Genome Wide Association Study ◽

Negative Impact ◽

Lateral Roots ◽

Primary Root ◽

Cytokinin Oxidase ◽

Cytokinin Signaling ◽

Organ Growth ◽

A Genome

AbstractDirectional organ growth allows the plant root system to strategically cover its surroundings. Intercellular auxin transport is aligned with the gravity vector in the primary root tips, facilitating downward organ bending at the lower root flank. Here we show that cytokinin signaling functions as a lateral root specific anti-gravitropic component, promoting the radial distribution of the root system. We performed a genome-wide association study and revealed that signal peptide processing of Cytokinin Oxidase 2 (CKX2) affects its enzymatic activity and, thereby, determines the degradation of cytokinins in naturalArabidopsis thalianaaccessions. Cytokinin signaling interferes with growth at the upper lateral root flank and thereby prevents downward bending. Our interdisciplinary approach revealed that two phytohormonal cues at opposite organ flanks counterbalance each other’s negative impact on growth, suppressing organ growth towards gravity and allow for radial expansion of the root system.

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