Low Temperature Affects Stem Cell Maintenance in Brassica oleracea Seedlings.

Jennifer De Jonge,Jan Kodde,Guusje Bonnema,Gerco C Angenent,Richard G H Immink,Steven P C Groot,Edouard I Severing

doi:10.3389/fpls.2016.00800

Abstract

Most of the above ground tissues in higher plants originate from stem cells located in the shoot apical meristem (SAM). Several plant species can suffer from spontaneous stem cell arrest resulting in lack of further shoot development. In Brassica oleracea this SAM arrest is known as blindness and occurs in an unpredictable manner leading to considerable economic losses for plant raisers and farmers. Detailed analyses of seedlings showed that stem cell arrest is triggered by low temperatures during germination. To induce this arrest reproducibly and to study the effect of the environment, an assay was developed. The role of genetic variation on the susceptibility to develop blind seedlings was analyzed by a quantitative genetic mapping approach, using seeds from a double haploid population from a cross between broccoli and Chinese kale, produced at three locations. The analysis revealed, besides an effect of the seed production location, a region on linkage group C3 associated with blindness sensitivity. A subsequent dynamic genome-wide transcriptome analysis resulted in the identification of around 3000 differentially expressed genes early after blindness induction. A large number of cell cycle genes were en masse induced early during the development of blindness, whereas shortly after, all were down-regulated. This miss-regulation of core cell cycle genes is accompanied with a strong reduction of cells reaching the DNA replication phase. From the differentially expressed genes, 90 were located in the QTL region C3. Among them are two genes belonging to the MINICHROMOSOMAL MAINTENANCE gene family, known to be involved in DNA replication, a RETINOBLASTOMA-RELATED gene, a key regulator for cell cycle initiation, and several MutS homologs genes, involved in DNA repair. These genes are potential candidates for being involved in the development of blindness in Brassica oleracea sensitive genotypes.

Highlights

Upon germination and during the vegetative stage of development, a small almost constant number of pluripotent stem cells is located in the shoot and root apical meristems (Yanai et al, 2005; van Zanten et al, 2011)
Since we identified Gene ontology (GO)-terms related to cell proliferation as being over-represented both at days 2 and 7 after cold treatment in seedlings from a blindness-sensitive line (AG5010; Supplementary Tables S5 and S6), we further focused on cell cycle related genes in the genome-wide transcriptome data set
We found that low temperature stress is a major trigger for shoot apical meristem (SAM) arrest in sensitive B. oleracea seedlings, since a high frequency of blind plants could be induced by about 10 days of incubation of fully imbibed seeds at 0–1◦C

Summary

Introduction

Upon germination and during the vegetative stage of development, a small almost constant number of pluripotent stem cells is located in the shoot and root apical meristems (Yanai et al, 2005; van Zanten et al, 2011). The shoot apical meristem (SAM) can be divided into a central zone that is essential for maintenance of the meristem and a peripheral zone, from which lateral organs are initiated (Jürgens, 1995). In the plant model species Arabidopsis thaliana, maintenance of central stem cells is organized by a feedback loop between WUSCHEL, a homeobox transcription factor, and CLAVATA receptor-like kinases and ligand proteins (Laux et al, 1996; Schoof et al, 2000). Plants have the ability to adapt to abiotic stress (e.g., temperature, drought, and salt) via specific signaling pathways involving phytohormones and regulatory proteins, such as receptors, protein modifiers, and transcription factors, leading to gene expression changes (Koornneef et al, 1991; Davis, 2009)

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