Comparative RNA-seq based transcriptome profiling of waterlogging response in cucumber hypocotyls reveals novel insights into the de novo adventitious root primordia initiation

Abstract

BackgroundWaterlogging is a serious abiotic stress to plant growth because it results in the decline in the supplement of oxygen to submerged tissues. Although cucumber (Cucumis sativus L.) is sensitive to waterlogging, its ability to generate adventitious roots (ARs) facilitates gas diffusion and increases plant survival when the oxygen concentration is decreased. To gain a better understanding of the molecular mechanisms that enable de novo AR primordia emergence upon waterlogging, the RNA sequencing-based transcriptomic responses of two contrasting cucumber genotypes, Zaoer-N (waterlogging tolerant) and Pepino (waterlogging sensitive), which differed in their abilities to form AR were compared.ResultsMore than 27,000 transcripts were detected in cucumber hypocotyls, from which 1494 and 1766 genes in ‘Zaoer-N’ and ‘Pepino’, respectively, were differentially expressed 2 days after waterlogging. The significant positive correlation between RNA sequencing data and a qPCR analysis indicated that the identified genes were credible. A comparative analysis revealed that genes functioning in carbohydrate mobilization, nitrate assimilation, hormone production and signaling pathways, transcription factors and cell division might contribute to the waterlogging-triggered AR primordia initiation. Ethylene was determined to be an important plant hormone responsible for the cucumber ARs initiation. Additionally, genes encoding cytochrome P450, ankyrin repeat-containing proteins and sulfite oxidases were determined as important in waterlogging acclimation.ConclusionThis research broadens our understanding of the mechanism underlying waterlogging-triggered ARs emergence, and provides valuable information for the breeding of cucumber with enhanced waterlogging tolerance.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-017-1081-8) contains supplementary material, which is available to authorized users.

The major‐effect quantitative trait locus CsARN6.1 encodes an AAA ATPase domain‐containing protein that is associated with waterlogging stress tolerance by promoting adventitious root formation

“…Waterlogging or flooding results in severe oxygen deficiency that compromises mitochondrial respiration and leads to an insufficiency in ATP for energy‐demanding processes (van Dongen et al ., ; Geigenberger, ; Bailey‐Serres and Voesenek, ; Zabalza et al ., ). Indeed, our previous proteomics and transcriptomic studies in Zaoer‐N and Pepino revealed that while the two lines exhibited a similar enzyme cascade as found in other plants in response to the waterlogging stress, Zaoer‐N was more efficient at regenerating ATP and NAD + and continuation of the glycolysis pathway to deal with the energy crisis from waterlogging (Xu et al ., , ). Typically, the AAA domain in the AAA ATPase has the conserved function of binding ATP and converting the energy from ATP hydrolysis into a force that promotes cell division, expansion, growth and development (Hicks‐Berger et al ., ; Huang et al ., ).…”

“…It is known that all plant hormones, especially auxin and ethylene, play important roles in AR formation (e.g. Steffens and Sauter, 2009;Vidoz et al, 2010), and this is also true for cucumber (Lanteri et al, 2006;Dong et al, 2016;Xu et al, 2017b). The genetic variation for AR development has been reported in Arabidopsis (King and Stimart, 1998;Zhang and Forde, 1998), Populus (Ribeiro et al, 2016) and several crop plants such as tomato (Arikita et al, 2013), Brassica napus (Oldacres et al, 2005), maize (Mano et al, 2005;Watanabe et al, 2017) and rice (Zheng et al, 2003;Ikeda et al, 2007).…”

“…We hypothesized that the gene(s) underlying ARN6.1 might be differentially expressed, resulting in phenotypic variation in ARN under waterlogging stress. In an earlier study, we examined the transcriptomes of Zaoer-N and Pepino hypocotyls under waterlogged treatments and the nonwaterlogged controls (Xu et al, 2017b). Transcripts of six of the seven genes in the 36.1-kb candidate gene region were present in the transcriptomes; however, only Csa6G504460 was significantly increased (about 1.5-fold) in waterlogged Zaoer-N compared with the non-waterlogged control, whereas no significant difference in its expression was found in Pepino ( Figure 3b).…”

A fast, simple, high efficient and one-step generation of composite cucumber plants with transgenic roots by Agrobacterium rhizogenes-mediated transformation

“…In 2016, gross production value is 40,229 million US$ (FAO). However, cucumber is high sensitive to low/high temperature, drought/waterlogging and salt stresses that cause significant reductions in yields (Liu et al 2013Ma et al 2018;Xu et al 2017Xu et al , 2018. In addition, a wide range of soilborne diseases (pathogenes), viruses and nematodes are one of the main constraints on cucumber production (Li and Chen 2017;Liang et al 2019;Liu et al 2017).…”

The auxin receptor TIR1 homolog (PagFBL 1) regulates adventitious rooting through interactions with Aux/IAA28 in Populus

“…Auxin signalling starts from the FBL1-mediated Aux/IAA degradation, prompting us to identify Aux/IAA proteins that might be targeted by PagFBL1. Aux/IAA genes exhibit differential expression under auxin treatment and are generally more responsive than ARF or TIR1/AFB genes (De Almeida et al, 2015;Ivan et al, 2008;Trenner et al, 2016;Villacorta-Mart ın et al, 2015;Wen et al, 2016;Xu et al, 2017a). We screened the candidate Aux/ IAA genes that showed changes in expression during the early stages of AR formation, or else show differential expression in WT control vs OE plants undergoing AR formation.…”