Rapid temperature responses of photosystem II efficiency forecast genotypic variation in rice vegetative heat tolerance

Abstract

A key target for the improvement of Oryza sativa (rice) is the development of heat-tolerant varieties. This necessitates the development of high-throughput methodologies for the screening of heat tolerance. Progress has been made to this end via visual scoring and chlorophyll fluorescence; however, these approaches demand large infrastructural investments to expose large populations of adult plants to heat stress. To address this bottleneck, we investigated the response of the maximum quantum efficiency of photosystem II (PSII) to rapidly increasing temperatures in excised leaf segments of juvenile rice plants. Segmented models explained the majority of the observed variation in response. Coefficients from these models, i.e. critical temperature (T crit) and the initial response (m 1), were evaluated for their usability for forecasting adult heat tolerance, measured as the vegetative heat tolerance of adult rice plants through visual (stay-green) and chlorophyll fluorescence (ɸPSII) approaches. We detected substantial variation in heat tolerance of a randomly selected set of indica rice varieties. Both T crit and m 1 were associated with measured heat tolerance in adult plants, highlighting their usability as high-throughput proxies. Variation in heat tolerance was associated with daytime respiration but not with photosynthetic capacity, highlighting a role for the non-photorespiratory release of CO 2 in heat tolerance. To date, this represents the first published instance of genetic variation in these key gas-exchange traits being quantified in response to heat stress in a diverse set of rice accessions. These results outline an efficient strategy for screening heat tolerance and accentuate the need to focus on reduced rates of respiration to improve heat tolerance in rice.

The potential of resilient carbon dynamics for stabilizing crop reproductive development and productivity during heat stress

“…PSII is the most heat‐sensitive component of photosynthetic biochemistry (Hu et al, 2020), as such reduced PSII activity is often the most common determiner of reduced photosynthesis (Tang et al, 2007). For this reason, chlorophyll fluorescence techniques are often employed to benchmark heat tolerance (Ferguson et al, 2020; Sharma, Andersen, Ottosen, & Rosenqvist, 2015; Sharma, Torp, Rosenqvist, Ottosen, & Andersen, 2017). High temperatures have also been shown to negatively affect the balance between photosynthesis and photorespiration, which in turn reduces the overall carbohydrate pool and ultimately yield (Prasad et al, 2017).…”

“…A sustained decline in PSII efficiency can be quickly assayed via dark‐adapted chlorophyll fluorescence (Murchie & Lawson, 2013), consequently assessing the maximum efficiency of PSII ( F v / F m ) under heat stress in reproductive structures has potential as a high‐throughput platform from which to gauge heat tolerance that will contribute to sustained reproductive development. To this end and as a proof of concept for this review, we employed our recently published approach of gauging F v / F m responses to incrementally increasing temperatures in rice leaves (Ferguson et al, 2020) to wheat ears undergoing grain‐filling of two distinct accessions (Figure 3). Here, we observed a significant difference in the maintenance of F v / F m under heat stress between the two accessions, which is likely to be driven by the previously described PSII responses to temperature that impairs electron transport.…”

“…Wheat ear photosynthetic responses to heat stress. Ears from two wheat genotypes (Borlaug and Cadenza) were subjected to rapid incremental increases in temperature with concurrent measurements of chlorophyll fluorescence following the protocol of Ferguson et al (2020). Data at two temperature points [34°C (top) and 46°C (bottom)] are shown.…”

“…Processes underlying photosynthesis, for example, electron transport (Ferguson et al, 2020) and Rubisco activation (Perdomo, Capó‐Bauçà, Carmo‐Silva, & Galmés, 2017), and reproductive development, for example, anther dehiscence (Jiang et al, 2019) and pollen tube growth (Shi et al, 2018), are sensitive to moderate‐to‐high temperature increases. Consequently, disruptions to these key growth and productivity determining processes underlie a substantial proportion of yield decreases during heat stress (Chaturvedi, Bahuguna, Di, Pal, & Jagadish, 2017; Prasad, Boote, Allen, Sheehy, & Thomas, 2006; Thomey, Slattery, Köhler, Bernacchi, & Ort, 2019).…”

Magnesium Application Promotes Rubisco Activation and Contributes to High-Temperature Stress Alleviation in Wheat During the Grain Filling

“…The factors directly limiting photosynthesis at different degrees of HTS remain controversial because the photosynthetic system produces varying responses at different temperature ranges (Salvucci and Crafts-Brandner, 2004b;Yamori et al, 2013). CE, V Cmax , and J max decreased under HTS (Weston and Bauerle, 2007;Ferguson et al, 2020). V Cmax decreased earlier than J max at 17DAA, whereas both decreased synchronously at 20DAA and 25DAA; thus, J max decreased after V Cmax inhibition.…”