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

Abstract

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.

Keywords: different plant parts; heat stress; potato; tuber development.

Figure 1

A schematic diagram of the heat-stress treatments for the different potato plant parts. (1) EN: a normal-temperature treatment on the entire plant; (2) UH: a high-temperature treatment on the underground part alone; (3) EH: a high-temperature treatment on the entire plant; (4) AH: a high-temperature treatment on the aerial part alone.

Figure 2

Phenotypes of the aerial plant parts of Qs9 (a) and D187 (b) under the heat-stress treatment of different plant parts. Potato plants were grown for 0, 1, 2, 7, or 11 weeks at the indicated temperature. Representative pictures among 9 replicates are displayed. w, weeks.

Figure 3

Measurement of stem phenotype and leaf angle under heat-stress treatment of different plant parts. (a–c) and (g–i): plant height (a), number of nodes (b), internode length (c), number of healthy leaves (g), leaf angle (h), and leaf drooping angle (i) of the Qs9 plants at the indicated time points during the treatment. (d–f) and (j–l): plant height (d), number of nodes (e), internode length (f), number of healthy leaves (j), leaf angle (k), and leaf drooping angle (l) of the D187 plants at the indicated time points during the treatment. In total, 10 replicates were averaged and statistically analysed. The different lowercase letters indicate groups that are significantly different from one another.

Figure 4

Potato tuberization of the Qs9 and D187 plants under the heat-stress treatment of different plant parts. Potato plants of the Qs9 (a) and D187 (b) cultivars were grown for 0, 1, 2, 7, or 11 weeks under heat-stress treatments of different parts of the plant. Photographs were taken after the removal of soil. Representative pictures among the nine replicates are displayed. Scale bars, 2 cm. The white arrow points to the tuber or stolon. w, weeks. (c–e): stolon number (c), tuber number (d), and tuber yield (e) per plant of the Qs9 cultivar at the indicated time points during the treatment. (f–h): stolon number (f), tuber number (g), and tuber yield (h) per plant of the D187 cultivar at the indicated time points during the treatment. Nine replicates were averaged and statistically analysed. (e,h) Graph inset showing an enlarged view of the tuber yield at 1 and 2 weeks. The different lowercase letters indicate groups that are significantly different from one another.

Figure 5

Phenotypes and tuber productivity of the Qs9 and D187 plants under the heat-stress treatment of different plant parts. (a,b): Photographs of the total tubers harvested from the nine plants. a: Qs9, b: D187. (c,d): Measurement of tuber productivity under the heat-stress treatments of different parts of the plants. Tuber yield (c) and tuber number (d) per plant; nine replicates were averaged and statistically analysed. The different lowercase letters indicate groups that are significantly different from one another. (e) The percentage of tuber numbers among the total number of tubers in the annotated range of fresh weight is displayed using a heatmap. The total number of tubers is the sum of the tuber numbers in all analysed potato plants in each treatment.

Figure 6

A Venn diagram showing the number of DEGs of the Qs9 (a) and D187 (b) plants under the heat-stress treatment of different plant parts. Genes with a log2-fold change greater than 1.5-fold and a p-value < 0.01 were considered DEGs.

Figure 7

The expression of the selected genes from the transcriptome analysis. Expression of the candidate genes involved in temperature-dependent tuberization. Red to blue indicates expression from high to low. The colour scale represents log₂ (FPKM+1).

Figure 8

The expression of selected genes from the Qs9 (a,b) and D187 (c,d) plants under the heat-stress treatment of different plant parts was determined by RT-qPCR. Activator (a,c) and repressor (b,d) genes of tuberization. Three replicates were averaged and statistically analysed. The different lowercase letters indicate groups that are significantly different from one another.