Elevated Temperatures Impose Transcriptional Constraints and Elicit Intraspecific Differences Between Coffee Genotypes

Abstract

The projected impact of global warming on coffee production may require the heatadapted genotypes in the next decades. To identify cellular strategies in response to warmer temperatures, we compared the effect of elevated temperature on two commercial Coffea arabica L. genotypes exploring leaf physiology, transcriptome, and carbohydrate/protein composition. Growth temperatures were 23/19°C (day/night), as optimal condition (OpT), and 30/26°C (day/night) as a possible warmer scenario (WaT). The cv. Acauã showed lower levels of leaf temperature (Tleaf) under both conditions compared to cv. Catuaı, whereas slightly or no differences for other leaf physiological parameters. Therefore, to explore temperature responsive pathways the leaf transcriptome was examined using RNAseq. Genotypes showed a marked number of differentially-expressed genes (DEGs) under OpT, however DEGs strongly decrease in both at WaT condition indicating a transcriptional constraint. DEGs responsive to WaT revealed shared and genotype-specific genes mostly related to carbohydrate metabolism. Under OpT, leaf starch content was greater in cv. Acauã and, as WaT temperature was imposed, the leaf soluble sugar did not change in contrast to cv. Catuaı, although the levels of leaf starch, sucrose, and leaf protein decreased in both genotypes. These findings revealed intraspecific differences in the underlying transcriptional and metabolic interconnected pathways responsive to warmer temperatures, which is potentially linked to thermotolerance, and thus may be useful as biomarkers in breeding for a changing climate.

A Transcriptomic Approach to Understanding the Combined Impacts of Supra-Optimal Temperatures and CO2 Revealed Different Responses in the Polyploid Coffea arabica and Its Diploid Progenitor C. canephora

“…Genome assembly of the allotetraploid C. arabica supports a high level of genetic sharing with the diploid progenitors, C. canephora and C. eugenioides [ 20 ]. Comparative studies between coffee species and genotypes are scarce, but the few existing ones are in line with our findings and suggest some common responses to supra-optimal temperatures [ 36 , 41 , 47 ] and a bottleneck effect in transcriptional activation at warmer temperatures [ 35 ]. On the other hand, eCO 2 increased the numbers at 42 °C in both genotypes ( Figure 2 ).…”

“…These DEGs are probably critical for enhancing temperature tolerance in Icatu and CL153, in contrast with other varieties of C. arabica (cv. Acauã and Catuaí) where the number of DEGs decreased as a response to elevated temperatures (23/19 °C vs. 30/26 °C [ 35 ]). Nevertheless, these differences might also be due to the short period of the experimental trial (e.g., 4 weeks [ 35 ] vs. 10 months in our present study), and to the physiological performance of coffee plants which is frequently higher at 30 °C than at 25 °C [ 14 , 30 ].…”

“…In the last 20 years, a considerable amount of research has been devoted to environmental coffee physiology focusing on water relations and drought tolerance mechanisms, but little is still known on the mechanisms of tolerance to unfavorable temperatures, namely transcriptional and metabolic differences in response to warmer temperatures (see [ 35 ]). For instance, it has been observed that in Coffea , eCO 2 promotes a high plant vigor [ 13 ] and even crop yield [ 36 ], while improving tolerance to drought [ 37 , 38 , 39 ] and supra-optimal temperatures [ 14 , 37 , 40 , 41 ], with positive impacts on the physical and chemical traits of the coffee beans under supra-optimal temperatures, contributing to preserve its quality [ 42 ].…”

Selenium enhances chilling stress tolerance in coffee species by modulating nutrient, carbohydrates, and amino acids content

“…These results are explained by the allopolyploidy of C. arabica , which promotes an evolutionary advantage in having additional genetic materials that attribute greater plasticity in coping with environmental variations compared with its parentals—in this case, C. canephora and C. eugenioides . In other words, the allopolyploidy of C. arabica makes this species able to up and downregulate certain genes responsible to keep the homeostasis during low temperatures, as reported by Bardil et al (2011) , or even at higher temperatures ( de Oliveira et al, 2020 ).…”

Protective Responses at the Biochemical and Molecular Level Differ between a Coffea arabica L. Hybrid and Its Parental Genotypes to Supra-Optimal Temperatures and Elevated Air [CO2]

“…Traditionally, the optimal annual mean temperature range was stated as 18–21 °C for arabica cultivars [ 50 ]. In this way, it was reported that mean air temperatures above 23 °C could accelerate fruit ripening of arabica cultivars, which can cause bean quality loss, and seasonal high temperatures above 33 °C and dryer seasons can greatly reduce floral initiation and increase the production of abnormal reproductive structures, and flower abortion [ 51 , 52 , 53 , 54 ]. However, current Arabica cultivars can grow in marginal regions, such as in the northeast of Brazil, where the mean annual temperature can reach 25 °C [ 55 ], and elite cultivars can successfully withstand relatively high temperatures [ 12 , 34 ] to a greater extent than traditionally assumed in classical studies [ 56 ].…”