Wound-inducible ANAC071 and ANAC096 transcription factors promote cambial cell formation in incised Arabidopsis flowering stems

Matsuoka, Katsuyoshi; Sato, Ryosuke; Matsukura, Yuki; Kawajiri, Y.; Iino, Hiromi; Nozawa, Naoyuki; Shibata, Kyomi; Kondo, Yuki; Satoh, Shinobu; Asahina, Masashi

doi:10.1038/s42003-021-01895-8

Cited by 38 publications

(27 citation statements)

References 46 publications

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“…To shed light on whether the orthologs of known graft-related genes have similar roles in both species, the expression of all tomato and pepper orthologs for functionally characterized, grafting- and vasculature-related genes from A. thaliana ( VND6 , VND7 , WOX4 , COTYLEDON VASCULAR PATTERN 2 [ CVP2 ], PXY , HCA2 , RAP2.6L , ABERRANT LATERAL ROOT FORMATION 4 [ ALF4 ], NAC DOMAIN CONTAINING PROTEIN 96 [ ANAC096 ], and ANAC071 ) were plotted from the self-grafted and heterografted data sets. Notably, these plots show highly perturbed expression in the heterografts, compared to the self-grafts ( Supplemental Figure S8 ; DiDonato et al, 2004 ; Ji et al, 2010 ; Sugimoto et al, 2010 ; Yamaguchi et al, 2010 ; Asahina et al, 2011 ; Pitaksaringkarn et al, 2014; Melnyk et al, 2018 ; Matsuoka et al, 2018 , 2021 ; Smit et al, 2020 ). To identify additional candidates with spatially or temporally dynamic expression patterns in the heterografts, we used a modified Shannon entropy (MSE) analysis that uncovered 34 TFs, 9 of which were previously identified in graft co-expression networks ( Supplemental Figures S9 and S10 and Supplemental Data Set S8 ; Xie et al, 2019 ).…”

Section: Resultsmentioning

confidence: 99%

“…Despite the long history and wide-spread use of grafting, only eight genes have been directly implicated in junction formation. These genes are involved in cell proliferation and vascular specification ( Asahina et al, 2011 ; Pitaksaringkarn et al, 2014 ; Matsuoka et al, 2018 , 2021 ; Melnyk et al, 2018 ; Notaguchi et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

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Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation

et al. 2021

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Grafting has been adopted for a wide range of crops to enhance productivity and resilience; for example, grafting of Solanaceous crops couples disease-resistant rootstocks with scions that produce high-quality fruit. However, incompatibility severely limits the application of grafting and graft incompatibility remains poorly understood. In grafts, immediate incompatibility results in rapid death, but delayed incompatibility can take months or even years to manifest, creating a significant economic burden for perennial crop production. To gain insight into the genetic mechanisms underlying this phenomenon, we developed a model system using heterografting of tomato (Solanum lycopersicum) and pepper (Capsicum annuum). These grafted plants express signs of anatomical junction failure within the first week of grafting. By generating a detailed timeline for junction formation, we were able to pinpoint the cellular basis for this delayed incompatibility. Furthermore, we inferred gene regulatory networks for compatible self-grafts and incompatible heterografts based on these key anatomical events, which predict core regulators for grafting. Finally, we examined the role of vascular development in graft formation and uncovered SlWOX4 as a potential regulator of graft compatibility. Following this predicted regulator up with functional analysis, we show that Slwox4 homografts fail to form xylem bridges across the junction, demonstrating that indeed, SlWOX4 is essential for vascular reconnection during grafting, and may function as an early indicator of graft failure.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation

et al. 2021

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“…In addition to cZ, we found high levels of ACC in the apical region of the explants at 24 hae, coinciding with extensive cell proliferation in this region. Downstream candidates for wound-induced cell proliferation are the AP2/ERF transcription factor WOUND INDUCED DEDIFFERENTIATION 1 (WIND1), which enhances endogenous CK responses in Arabidopsis [56], and ANAC071, which is induced by ethylene and that triggered cell proliferation of the cambial initials during wound healing in Arabidopsis flowering stems [57,58]. Additional experiments will be required to address whether similar regulatory networks are involved in wound-induced de novo organ formation in 'Micro-Tom' hypocotyl explants and to confirm the pivotal role of photorespiration for adventitious shoot formation [9].…”

Section: Discussionmentioning

confidence: 99%

Dynamic Hormone Gradients Regulate Wound-Induced de novo Organ Formation in Tomato Hypocotyl Explants

Larriba

Sánchez-García

Justamante

et al. 2021

IJMS

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Plants have a remarkable regenerative capacity, which allows them to survive tissue damage after biotic and abiotic stresses. In this study, we use Solanum lycopersicum ‘Micro-Tom’ explants as a model to investigate wound-induced de novo organ formation, as these explants can regenerate the missing structures without the exogenous application of plant hormones. Here, we performed simultaneous targeted profiling of 22 phytohormone-related metabolites during de novo organ formation and found that endogenous hormone levels dynamically changed after root and shoot excision, according to region-specific patterns. Our results indicate that a defined temporal window of high auxin-to-cytokinin accumulation in the basal region of the explants was required for adventitious root formation and that was dependent on a concerted regulation of polar auxin transport through the hypocotyl, of local induction of auxin biosynthesis, and of local inhibition of auxin degradation. In the apical region, though, a minimum of auxin-to-cytokinin ratio is established shortly after wounding both by decreasing active auxin levels and by draining auxin via its basipetal transport and internalization. Cross-validation with transcriptomic data highlighted the main hormonal gradients involved in wound-induced de novo organ formation in tomato hypocotyl explants.

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“…As revealed by vascular differentiation patterns of primary root and leaf veins in Arabidopsis, NAC101/VND6 and NAC030/VND7 are key regulators of xylem differentiation ( Kubo et al, 2005 ), whereas NAC020, NAC045, and NAC086 participate in phloem differentiation ( Furuta et al, 2014 ; Kondo et al, 2016 ). In addition, NAC071 and NAC096 transmit auxin and ethylene signals, triggering xyloglucan endotransglucosylase/hydrolase cell wall organization, and promoting cambial cell formation after wounding ( Pitaksaringkarn et al, 2014 ; Matsuoka et al, 2021 ). Although these patterns were observed in Arabidopsis, there are similar patterns in other species ( Melnyk et al, 2018 ; Cui et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Conserved Regulatory Pathways for Stock-Scion Healing Revealed by Comparative Analysis of Arabidopsis and Tomato Grafting Transcriptomes

et al. 2022

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Many plants can successfully join root and shoot sections at cut surfaces when severed at the stem. Graft healing is complex and conserved in diverse taxonomic groups with different vascular structures. Herein, we compared transcriptome data from autografted and separated stem sections of Arabidopsis thaliana and tomato (Solanum lycopersicum) to explore changes related to graft healing. Using orthologous gene pairs identified between the two species, temperal expression patterns of evolutionary associated genes in grafted top and bottom, separated top and bottom, and intact stems were exhibited. Genes with expression preference indicate functional diversification of genes related to anatomical structure and cellular development in the two species. Expression profiles of the variable genes revealed common pathways operating during graft healing, including phenylpropanoid metabolism, response to oxygen-containing compounds, xylan, and cell wall biogenesis, mitosis and the cell cycle, carboxylic acid catabolism, and meristem structural organization. In addition, vascular differentiation related NAC domain transcription factors and genome-wide members in Arabidopsis and tomato were used for phylogenetic and expression analysis. Expression differences were largely consistent with sequence differences, reflecting high similarity for protein-coding and regulatory regions of individual clades. NAC proteins mainly clustered in accordance with their reported functions in xylem differentiation or cambium formation. The putative conserved mechanisms suggested by conserved genes and functions could help to expand graft healing theory to a wider range of species, and temporal fluctuations in common pathways imply conserved biological processes during graft healing.

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Wound-inducible ANAC071 and ANAC096 transcription factors promote cambial cell formation in incised Arabidopsis flowering stems

Cited by 38 publications

References 46 publications

Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation

Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation

Dynamic Hormone Gradients Regulate Wound-Induced de novo Organ Formation in Tomato Hypocotyl Explants

Conserved Regulatory Pathways for Stock-Scion Healing Revealed by Comparative Analysis of Arabidopsis and Tomato Grafting Transcriptomes

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