Arabidopsis QTLs Associated with Reduction of Fertility in Response to Heat Stress

Plants cope with seasonal and daily fluctuations in temperature, but when the temperature climbs from the tolerable range into the heat stress range, by ∼5°C above optimal conditions, cellular changes including increased membrane fluidity induce production of heat shock proteins, phytohormones, and protective factors, such as antioxidants and osmolytes (reviewed in Bita and Gerats, 2013). To mitigate problems caused by protein aggregation, the plant cells also make proteases, chaperones, and late embryogenesis-abundant proteins. The large numbers of potential responders reflect the importance of the response and the complexity of plant genomes; however, identifying potential targets for breeding or other approaches to improve heat tolerance remains challenging.

The effects of heat stress vary among species and among individuals in the same species; the effects also vary depending on the timing of the heat stress. Transcriptome analysis profiles the entire response to heat, but genetic analysis can pinpoint the factors that regulate the response to heat. To identify Arabidopsis thaliana quantitative trait loci (QTLs) modulating the effect of heat on reproduction, Bac-Molenaar et al. (2015) measured silique length following a 1-d heat stress treatment at 35°C. Because the Arabidopsis inflorescence has flowers at many stages of development, examination of siliques in different regions (see figure) allowed the authors to examine the heat response at different developmental stages. Examination of >250 natural accessions of Arabidopsis showed different regions were affected in different accessions. In many accessions, regions B, C, and D were sensitive to heat, indicating a strong effect on meiosis, fertilization, and early embryogenesis; by contrast, regions A and E showed little effect of heat treatment, indicating that late embryogenesis and early flower development tolerate heat stress better than other stages.

Quantifying the effects of heat on reproduction. Outline of control (A) and heat-treated (B) samples. The blue and red lines mark the first flower that opened on the day the plants were treated. The regions (10 siliques each) correspond to different developmental processes that were underway during the heat treatment: late embryogenesis (A), fertilization and early embryogenesis (B), preanthesis development and female meiosis (C), and male meiosis (D). After the siliques completed development, the length of each silique was measured; short siliques can be seen in zone D in the treated sample. (Reprinted from Bac-Molenaar et al. [2015], Figure 2.)

To examine the genetic underpinnings of this effect, the authors conducted genome-wide association analysis, which identified four QTLs associated with the response to heat stress. These QTLs showed their effects in different regions, indicating specific effects at different developmental stages. The authors next looked for candidate genes within the QTL interval and, where possible, tested loss-of-function mutations in the candidate genes to attempt to validate their potential effect on heat tolerance. For example, one QTL affecting preanthesis heat sensitivity may be caused by variation in QUASIMODO-LIKE2, which shows strong expression in male gametophyte development in region D. Examination of additional candidates, including MYO-INOSITOL 1-PHOSPHATE SYNTHASE3, FLOWERING LOCUS C, and others (but, surprisingly, no heat shock proteins), indicated a possible connection between heat stress responses and flowering time, as well as a potential role for pollen allergens.

We don’t need to review statistics on world population or predictions on climate change to understand that heat tolerance in crop plants provides an important target for plant breeding. Although the Arabidopsis QTLs identified here do not provide immediate, breeding-ready alleles for crop improvement, their identification does inform work to identify such alleles, or alternative approaches, in key crops. Integrating such alleles into elite crop varieties such that they improve heat tolerance in field conditions without causing detrimental effects may be a long way off, but this study moves us in the right direction.