Temporally distinct regulatory pathways coordinate thermo-responsive storage organ formation in potato

Park, Ji-Sun; Park, Su‐Jin; Kwon, Suk‐Yoon; Shin, Ah-Young; Moon, Ki-Beom; Park, Jeong Mee; Cho, Hye Sun; Park, Sang Un; Jeon, Jun Ho; Kim, Hyun-Soon; Lee, Hyo‐Jun

doi:10.1016/j.celrep.2022.110579

Cited by 23 publications

(48 citation statements)

References 43 publications

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“…Heat induced the expression of StSUT4 in the leaves and stolons of the HS genotype, which might have led to the activation of the StCOL1-StSP5G regulatory module. Such studies are consistent with the recent finding that elevated temperature caused higher StCOL1 accumulation and suppressed potato tuberization (Park et al, 2022). Our expression analysis revealed the higher expression of StSP5G transcript under high temperature in the HS genotype.…”

Section: Discussionsupporting

confidence: 93%

“…Furthermore, high temperature causes SP6A repression by a micro-RNA named SUPPRESSING OF SP6A (SES; Lehretz et al, 2019 ). Also, recently it has been shown that SP6A is suppressed transcriptionally and post-transcriptionally under high-temperature stress (Park et al, 2022 ). Epigenetic components are also involved in potato tuberization, wherein Polycomb Repressive Complex (PRC)-mediated histone modifications repress several target genes by H3K27 trimethylation (Kumar et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…The expression levels of StSP5G and StSP6A are usually difficult to interpret in vegetative tissues like stolons and tubers (Hancock et al, 2014 ). In addition, different regulatory pathways operate for photoperiod and temperature-dependent tuberization, suggesting that a complex regulatory network is involved in the regulation of potato tuberization (Park et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

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The interplay of DNA methyltransferases and demethylases with tuberization genes in potato (Solanum tuberosum L.) genotypes under high temperature

et al. 2022

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Potato is a temperate crop consumed globally as a staple food. High temperature negatively impacts the tuberization process, eventually affecting crop yield. DNA methylation plays an important role in various developmental and physiological processes in plants. It is a conserved epigenetic mark determined by the dynamic concurrent action of cytosine-5 DNA methyltransferases (C5-MTases) and demethylases (DeMets). However, C5-MTases and DeMets remain unidentified in potato, and their expression patterns are unknown under high temperatures. Here, we performed genome-wide analysis and identified 10 C5-MTases and 8 DeMets in potatoes. Analysis of their conserved motifs, gene structures, and phylogenetic analysis grouped C5-MTases into four subfamilies (StMET, StCMT3, StDRM, and StDNMT2) and DeMets into three subfamilies (StROS, StDML, and StDME). Promoter analysis showed the presence of multiple cis-regulatory elements involved in plant development, hormone, and stress response. Furthermore, expression dynamics of C5-MTases and DeMets were determined in the different tissues (leaf, flower, and stolon) of heat-sensitive (HS) and heat-tolerant (HT) genotypes under high temperature. qPCR results revealed that high temperature resulted in pronounced upregulation of CMT and DRM genes in the HT genotype. Likewise, demethylases showed strong upregulation in HT genotype as compared to HS genotype. Several positive (StSP6A and StBEL5) and negative (StSP5G, StSUT4, and StRAP1) regulators are involved in the potato tuberization. Expression analysis of these genes revealed that high temperature induces the expression of positive regulators in the leaf and stolon samples of HT genotype, possibly through active DNA demethylation and RNA-directed DNA methylation (RdDM) pathway components. Our findings lay a framework for understanding how epigenetic pathways synergistically or antagonistically regulate the tuberization process under high-temperature stress in potatoes. Uncovering such mechanisms will contribute to potato breeding for developing thermotolerant potato varieties.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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The interplay of DNA methyltransferases and demethylases with tuberization genes in potato (Solanum tuberosum L.) genotypes under high temperature

et al. 2022

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“…Meanwhile, tuberous roots mainly grow from the development of the primary cambium, followed by active cell division and cell expansion in the vascular cylinder [ 6 ]. The development of underground storage organ formation is initiated by a complex molecular biology process, which is controlled by environmental factors such as nutrient content, photoperiod, and temperature [ 7 , 8 , 9 ].…”

Section: Introductionmentioning

confidence: 99%

PEBP Signaling Network in Tubers and Tuberous Root Crops

Susila

Purwestri²

2023

Plants

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Tubers and tuberous root crops are essential carbohydrate sources and staple foods for humans, second only to cereals. The developmental phase transition, including floral initiation and underground storage organ formation, is controlled by complex signaling processes involving the integration of environmental and endogenous cues. FLOWERING LOCUS T (FT) and TERMINAL FLOWER 1/CENTRORADIALIS (TFL1/CEN), members of the phosphatidylethanolamine-binding protein (PEBP) gene family, play a central role in this developmental phase transition process. FT and FT-like proteins have a function to promote developmental phase transition, while TFL1/CEN act oppositely. The balance between FT and TFL1/CEN is critical to ensure a successful plant life cycle. Here, we present a summarized review of the role and signaling network of PEBP in floral initiation and underground storage organ formation, specifically in tubers and tuberous root crops. Lastly, we point out several questions that need to be answered in order to have a more complete understanding of the PEBP signaling network, which is crucial for the agronomical improvement of tubers and tuberous crops.

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“…Lehretz et al (2019) found that high temperature caused a small RNA that was suppressing the expression of SP6A ( SES ) to accumulate and inhibit StSP6A expression and that after SES was inhibited by the short tandem target mimic (STTM) method, StSP6A expression and tuber formation remained normal at a high temperature [ 17 ]. Recently, Park et al (2022) reported that the level of StSP6A transcription is repressed by various regulatory pathways in the early and late stages of heat stress, with posttranscriptional regulation in the early stage and transcriptional repression in the later stage [ 18 ].…”

Section: Introductionmentioning

confidence: 99%

Responses of Aerial and Belowground Parts of Different Potato (Solanum tuberosum L.) Cultivars to Heat Stress

Zhou

et al. 2023

Plants

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The mechanism of potato (Solanum tuberosum L) thermotolerance has been the focus of intensive research for many years because plant growth and tuber yield are highly sensitive to heat stress. However, the linkage between the aerial and belowground parts of potato plants in response to high temperatures is not clear. To disentangle this issue, the aerial and belowground parts of the heat-resistant cultivar Dian187 (D187) and the heat-sensitive cultivar Qingshu 9 (Qs9) were independently exposed to high-temperature (30 °C) conditions using a special incubator. The results indicated that when the belowground plant parts were maintained at a normal temperature, the growth of the aerial plant parts was maintained even when independently exposed to heat stress. In contrast, the treatment that independently exposed the belowground plant parts to heat stress promoted premature senescence in the plant’s leaves, even when the aerial plant parts were maintained at a normal temperature. When the aerial part of the plant was independently treated with heat stress, tuberization belowground was not delayed, and tuberization suppression was not as severe as when the belowground plant parts independently underwent heat stress. Heat stress on the belowground plant parts alone had virtually no damaging effects on the leaf photosynthetic system but caused distinct tuber deformation, secondary growth, and the loss of tuber skin colour. Transcriptome analysis revealed that the treatment of the belowground plant parts at 30 °C induced 3361 differentially expressed genes in the Qs9 cultivar’s expanding tubers, while the D187 cultivar had only 10,148 differentially expressed genes. Conversely, when only the aerial plant parts were treated at 30 °C, there were just 807 DEGs (differentially expressed genes) in the D187 cultivar’s expanding tubers compared with 6563 DEGs in the Qs9 cultivar, indicating that the two cultivars with different heat sensitivities have distinct regulatory mechanisms of tuberization when exposed to heat stress. The information provided in this study may be useful for further exploring the genes associated with high-temperature resistance in potato cultivars.

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Temporally distinct regulatory pathways coordinate thermo-responsive storage organ formation in potato

Cited by 23 publications

References 43 publications

The interplay of DNA methyltransferases and demethylases with tuberization genes in potato (Solanum tuberosum L.) genotypes under high temperature

The interplay of DNA methyltransferases and demethylases with tuberization genes in potato (Solanum tuberosum L.) genotypes under high temperature

PEBP Signaling Network in Tubers and Tuberous Root Crops

Responses of Aerial and Belowground Parts of Different Potato (Solanum tuberosum L.) Cultivars to Heat Stress

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