Rice responses to rising temperatures--challenges, perspectives and future directions.

Running title - Rice responses to rising temperatures

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Title - Rice responses to rising temperatures – challenges, perspectives and future directions

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Jagadish S V K1 *, Murty M V R1, Quick W P1,2 1 International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines 2 Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK *Corresponding author - Jagadish SVK, International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines; phone: +63 (2) 580-5600-2767; fax: +63 (2) 580-5699; 845-0606, email: [email protected]

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/pce.12430

1 This article is protected by copyright. All rights reserved.

Abstract

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Phenotypic plasticity in overcoming heat stress−induced damage across hot tropical rice-growing

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regions is predominantly governed by relative humidity. Expression of transpiration cooling, an

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effective heat-avoiding mechanism, will diminish with the transition from fully-flooded paddies

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to water-saving technologies such as direct-seeded and aerobic rice cultivation, thus further

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aggravating stress damage. This change can potentially introduce greater sensitivity to previously

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unaffected developmental stages such as floral meristem (panicle) initiation and spikelet

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differentiation, and further intensify vulnerability at the known sensitive gametogenesis and

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flowering stages. More than the mean temperature rise, increased variability and a more rapid

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increase in nighttime temperature compared with the daytime maximum present a greater

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challenge. This review addresses (i) the importance of vapor pressure deficit under fully flooded

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paddies and increased vulnerability of rice production to heat stress or intermittent occurrence of

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combined heat and drought stress under emerging water-saving rice technologies, (ii) the major

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disconnect with high night temperature response between field and controlled environments in

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terms of spikelet sterility, (iii) highlight the most important mechanisms that affect key grain

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quality parameters such as chalk formation under heat stress and, finally, (iv) we model and

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estimate heat stress−induced spikelet sterility taking South Asia as a case study.

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Key words – flowering, high temperature, relative humidity, rice, spikelet fertility, water-saving

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technologies

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Introduction

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Rice (Oryza sativa L.) traditionally has been grown as a fully flooded crop and has been the

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major source of calories for more than half the world’s population and livelihood of many small

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and marginal farmers of Asia and increasingly in Africa. With a significant jump in rice

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production during the 1960s (Green Revolution), followed by stagnation during the late 1990s, it

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is evident that increasing productivity is essential to keep pace with the demographic demand. In

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addition, global climatic predictions, of late with greater certainty, indicate increased frequency

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of heat spikes and warmer nights (IPCC, 2013), exerting additional challenges towards achieving

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higher crop yields. Considering the global harvested area, climate models predict that, by 2030,

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16% of the rice-growing area would be exposed to at least 5 days of temperatures above the

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critical threshold during the reproductive period, with a non-linear increase to 27% by 2050

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(Gourdji et al. 2013). Similarly, a global heat risk map for 2071–2100, with 1971−2000 as a

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reference, involving short episodes of heat stress coinciding with the reproductive period,

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resulted in more than 120 million ha of suitable wetland rice area to be under threat (Teixeira et

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al. 2013). Publications by Teixeira et al. (2013), Battisti & Naylor 2009 and Challinor et al.

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(2014) support the urgent need to enhance research efforts towards developing tolerant varieties

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and suitable crop management practices as adaptation strategies to minimize predicted damage.

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Further, rice yields having opposing sensitivity to daytime maximum and nighttime minimum

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temperature across South and Southeast Asia have been documented (Welch et al. 2010), with

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the latter accounting for a larger proportion of losses under field conditions (Peng et al. 2004;

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Welch et al. 2010; Nagarajan et al. 2010). Hence, increasing night (minimum) temperatures can

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potentially have a global impact compared with maximum day temperature, with the latter


posing a threat only to those locations that are already close to their optimal growing temperature

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(Prasad et al. 2006). In addition, a disproportional increase in night temperatures would reduce

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the diurnal amplitude, bringing with it a suite of negative impacts on crop production (Bueno et

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al. 2012).

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Rice is extremely sensitive to heat stress (>35 oC), particularly during the gametogenesis

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(Jagadish et al. 2013) and flowering (Prasad et al. 2006, Jagadish et al. 2007, 2008, 2010) stages,

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while information on other developmental stages such as early floral meristem growth, spikelet

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differentiation and grain filling are limited. The ability of rice to be highly productive even under

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temperatures >40 oC (higher than the defined critical threshold) across hot tropical countries such

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as Pakistan and Senegal is largely driven by a sufficient and timely availability of irrigation

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water, complemented by low relative humidity (RH). This helps plants to maintain their tissue

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temperature well below the critical threshold due to efficient transpiration-mediated cooling

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(Weerakoon et al. 2008; Wassmann et al. 2009; Julia & Dingkuhn, 2013). A 6 oC lower panicle

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temperature under well-irrigated arid climates of Australia (Matsui et al. 2007) and 4 oC higher

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panicle temperature under hot and humid conditions in China (Tian et al. 2010) substantiate the

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critical role played by RH when dealing with heat stress. The recent finding of high night

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temperature (HNT) under field conditions affecting grain quality through a reduced non-

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structural carbohydrate pool size (Shi et al., 2013) poses questions about source-sink dynamics

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and proportional damage caused by increased dark respiration. This would add to the challenges

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of increased stress during early grain development, resulting in less rice production and lower

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grain quality, leading to a significant reduction in economic benefits (Lyman et al., 2013).

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In addition to the projected increase in temperature, increased uncertainty in precipitation

patterns resulting in fewer rainy days along with the rapid expansion of urbanization and


industrialization in developing countries adds to the challenges faced by flooded rice production.

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Water-saving rice technologies such as direct-seeded rice and aerobic rice (Bouman et al. 2005,

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2007) are considered as potential options to sustain rice production, with alternate wetting and

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drying feasible only in areas with sufficient and timely availability of water, a luxury that most

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rice-growing regions do not possess. The transition from water-sufficient scenarios to water-

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saving methods can potentially change the entire cropping system dynamics such as increased

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weed pressure (Kumar & Ladha, 2011; Mahajan et al. 2013), nematode severity (Kreye et al.

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2009a, b) and other soil-related problems (Nie et al. 2007, 2009). This shift could expose

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previously unaffected developmental stages such as floral meristem initiation (panicle initiation)

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to damaging levels of heat stress, a key developmental phase that determines overall sink size

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and, hence, potential yield. In addition, the already known heat-sensitive reproductive stages

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such as gametogenesis and flowering will come under a higher intensity of exposure to heat

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stress. It is almost certain that tropical rice-growing regions will persist in future climate

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scenarios, with a higher evaporative demand wherein temperature-driven drought stress would

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feature as a built-in phenomenon. This needs to be addressed if we are to avoid catastrophic

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damage, especially when combined heat and drought stress coincide with the key developmental

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stages described above. A recent study documents the role of extreme heat in increasing demand

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for soil water to sustain carbon assimilation, and consequently reducing water availability during

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the later stages of growth due to enhanced evapo-transpiration (Lobell et al., 2013). Insufficient

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water availability then leads to a significant increase in tissue temperature that exacerbates the

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problem (Rizhsky et al., 2002; Jagadish et al., 2011).

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Hence, the objectives of this review are to examine:


(i)

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The importance of vapor pressure deficit under fully flooded paddies and

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increased vulnerability of rice production to heat stress or intermittent

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occurrence of combined heat and drought stress under emerging water-saving

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rice technologies.

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(ii)

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(iii)

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(iv)

The major disconnect with high night temperature response between field and controlled environments in terms of spikelet sterility. Highlight the most important mechanisms that affect key grain quality parameters such as chalk formation under heat stress. Modeling of the heat stress−induced reduction in spikelet fertility, taking South Asia as a case study.

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Past, present and future dimensions of the impact of heat stress on rice

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Prior to the late 1990s, very little attention was given to increasing temperature and in particular

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the negative impact on rice yield and grain quality. There has been a series of IPCC global

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climate change estimates over the last decade, coupled with an improvement in the precision of

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projections on temperature increases in the future (IPCC, 2013). There is also significant

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evidence that an increase in high temperature will result in major crop losses even under current

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climates (Kadam et al. 2014 and references within). These data have essentially elevated the

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importance of addressing the effects of temperature within a future climate change scenario. It is

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only recently that significant rice yield losses, induced by heat stress have been documented in

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the major rice-producing regions of China (Li et al. 2004), Japan (Hasegawa et al. 2009), the

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Philippines (Peng et al. 2004) and across South and Southeast Asia (Welch et al. 2010). In

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addition, mapping exercises have identified the regional vulnerability of rice when grown under

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conditions closer to the critical heat stress threshold in tropical and subtropical regions of South


and Southeast Asia (Wassmann et al. 2009) and at a global scale (Teixeira et al. 2013). Future

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temperature predictions have been shown to have a much greater impact on the minimum night

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temperature compared with the effect on the maximum day temperature, hence reducing the

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diurnal temperature amplitude (Vose et al. 2005). The frequency of occurrence of temperatures

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beyond defined thresholds was geographically mapped to identify vulnerable rice-growing

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regions with high day temperature (HDT) stress, HNT stress or a combination of both (Laborte et

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al. 2012). These data indicate large variability in the regional occurrence of stress and the change

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in diurnal temperature amplitude. Currently, the available literature related to the impacts of heat

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stress, the mechanisms that lead to damage (Jagadish et al. 2010, 2013, Prasad et al. 2006) and

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the subsequent economic losses (Lyman et al. 2013) is well documented for flooded rice

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conditions. A significant strain on the availability of labour and water has already started to

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emerge as a major reason for a possible shift to use less water and labour for rice production,

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thus requiring alternative cropping technologies such as direct-seeded rice and aerobic rice.

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Under flooded rice systems, gametogenesis and flowering are identified as the two most

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sensitive stages to HDT stress (Yoshida et al. 1981; Jagadish et al. 2007, 2010, 2013). Earlier

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developmental stages, such as floral meristem initiation and spikelet differentiation, are better

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protected because of the buffering layer of floodwater. In fact, the process of floral meristem

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initiation and its early development that also determines total spikelet number is completed under

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water. Higher ambient temperatures, even up to 39 oC under controlled-environment conditions,

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did not result in a reduction in either spikelet number or spikelet fertility across five different rice

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cultivars (Fig. 1). Data obtained from thermocouples indicated that the increase in water and soil

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temperature was significantly lower than the prevailing ambient air temperature and that the

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increase in water temperature may be well below the critical threshold (which is unknown)


affecting the initiating floral meristem (Fig. 2A, Jagadish et al. UnPub). Considering future

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climate scenarios, in which a larger proportion of rice cultivation would be more mechanized and

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under direct-seeded or aerobic conditions, the luxury of the water layer protecting initial

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meristem growth could be challenged by higher soil and tissue temperatures. A study involving

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fully flooded transplanted paddy and direct-seeded rice (DSR) recorded up to 25% shorter plants

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in a DSR system. The internal competition from a much higher seeding density with DSR leads

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to a significant delay in canopy cover, thus exposing the soil to increased temperature for longer

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durations. This would lead to a similar condition termed “noise” that is observed when taking

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thermal images to quantify crop canopy temperature under conditions of much hotter soil

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temperature (see Fig. 5 in Munns et al. 2010). Hence, the increase in temperature just above or at

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the ground surface, close to the initiating panicle, could potentially expose this sensitive stage to

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much greater temperatures than in flooded conditions, thereby increasing its vulnerability. Under

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DSR, even a 10 kPa soil water tension (not considered a stress – Kumar & Ladha, 2011)

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maintained throughout the crop growth period resulted in a 53% reduction in spikelet number.

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This caused a serious reduction in overall sink size among main tiller panicles even under a non-

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stress (10 kPa) condition but recorded no reduction in grain-filling percentage (Supplementary

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Figure S1; Quinnones et al. UnPub). However, the proportion of the decline in sink size that can

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be compensated for by a greater number of plants per unit area, under direct-seeded conditions,

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needs to be quantified. Recently, higher temperatures, which increase vapor pressure deficit

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(conditions prevailing with combined high temperature and low relative humidity) and hence

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transpiration, were shown to advance severe drought stress in maize (Lobell et al. 2013).

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Imposing drought stress during pre-anthesis resulted in a significant reduction in both seed-set

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and abortion in primary rachis branches and more strongly in secondary rachis branches in rice


(Kato et al. 2008). Hence, the sensitive floral meristem and spikelet differentiation stage already

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vulnerable with the transition from fully flooded conditions to non stress (10 kPa) direct-seeded

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system (Supplementary Figure S1), when exposed to higher soil temperatures, or combined

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drought and heat stress, could emerge as a new vulnerable developmental stage under future

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climates. This warrants detailed investigation to ascertain the level of damage caused and the

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appropriate measures to overcome such damage.

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Flowering is identified as the most sensitive development stage to heat stress, with pollen

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viability being the major yield-determining factor (Yoshida et al. 1981; Jagadish et al. 2010).

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The crucial role of transpiration cooling overcoming heat stress−induced spikelet sterility has

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been highlighted earlier (Weerakoon et al. 2008; Wassmann et al. 2009; Julia & Dingkuhn,

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2013). A transition towards water-saving technologies would automatically deprive rice plants of

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this plasticity to respond to high temperature stress either partially or completely depending on

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the availability of water. This would increase the canopy or panicle tissue temperature by about 2

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o

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flowering is a novel strategy identified and exploited in the flooded rice system to overcome the

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damaging effects of high temperature stress by advancing the peak flowering time towards dawn

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when the temperature is cooler (Ishimaru et al. 2010). An extension of this trait into DSR

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cultivars could partially reduce the impact of high temperatures occurring during the late

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morning and near noon. On the other hand, an increase in panicle and overall canopy

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temperature would hasten crop senescence, thus decreasing both crop duration and grain filling

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as shown in wheat (Lobell et al. 2012). Grain-filling duration in tropical rice varieties is already

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shorter than in temperate cultivars and, with a further stress-induced decrease in grain-filling

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duration, this could potentially lead to a significant decrease in grain quantity and quality due to

C, even under non-stress (10 kPa) conditions (Fig. 2b; Quinones et al. UnPub). Early morning


increased chalk formation (Lyman et al. 2013). In summary, the otherwise well-protected floral

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meristem initiation under flooded rice cultivation could emerge as another highly vulnerable

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stage under the proposed use of water-saving technologies. In addition, the transition could cause

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greater damage to seed-set and early grain filling because of higher canopy temperatures. These

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changes present additional challenges to overcome, if we are to sustain rice yield and quality

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under the predicted hotter climates of the future.

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Mechanisms driving HDT- and HNT-induced rice yield and quality losses

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At the global (Vose et al. 2005), country (Zhou et al. 2004; Rao et al. 2014) and farm level

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(Peng et al. 2004), a much greater increase in the minimum night temperature over the maximum

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day temperature has been documented and supported by the recent IPCC (2013) report. Research

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focused on addressing the impact of HDT stress has made significant progress in using heat-

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tolerant donors such as rice landrace N22, developing mapping populations, identifying QTLs

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and developing heat-tolerant NILs that are currently used to enhance tolerance of HDT stress

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(Jagadish et al. 2010, Ye et al. 2012). Mechanistically, the major damage caused by HDT to rice

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either at anthesis or gametogenesis is a reduction in pollen viability and pollen tube growth,

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translating into lower spikelet fertility (Jagadish et al. 2010, 2013). The recent literature from

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controlled-environment studies with HNT treatments also records stress impacts on rice and the

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conclusions drawn indicate a similar phenomenon of decreased pollen viability, leading to

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spikelet sterility, as the major cause (Mohammed & Tarpley, 2009 a, b, 2010, 2011, 2013; Cheng

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et al. 2009). Other associated traits have also been reported such as increased respiratory losses,

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increased oxidative damage and decreased membrane stability (Mohammed & Tarpley, 2009a).

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It has to be noted that all of these results are generated from controlled environments. HNT

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resulting in yield losses under field conditions is documented to be around 23 or 24 oC (Peng et

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al. 2004; Nagarajan et al. 2010) and 28 oC (Shi et al., 2013), whereas this is measured to be ≥32

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o

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has been a tendency to use thresholds for examining HNT responses by imposing temperature

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treatments that are closer to HDT thresholds (35 oC; Jagadish et al. 2007, 2008). This is mainly

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due to the lack of a well-defined critical HNT threshold, which has resulted in finding similar

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physiological mechanisms that are susceptible to HDT stress, i.e. lower spikelet fertility and

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yield losses. Two reasons why these conclusions need more thorough investigation is that almost

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all studies have restricted their analysis to individual cultivars and they also use very high night

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temperatures. The observed effects could also have more to do with extremely low diurnal

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C in controlled chambers (Mohammed & Tarpley, 2009 a, b, 2010; Cheng et al. 2009). There

temperature amplitude than with HNT per se. Unlike the previously published literature, a study carried out under unique field-based

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HNT tents exposing rice plants to HNT from panicle initiation to maturity recorded no losses in

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spikelet fertility in both stress-tolerant and susceptible cultivars (Shi et al. 2013). Shi et al (2013)

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demonstrated that the heat treatment caused a significant decline in overall biomass and reduced

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non-structural carbohydrate (NSC) content in plant tissues, including the panicle, and resulted in

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decreased grain weight through reduced grain width, ultimately resulting in yield and grain

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quality losses. This study clearly indicates the differential responses of rice plants exposed to

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HDT and HNT, with a different chain of processes leading to HNT damage under field

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conditions. To further substantiate this claim, we have taken the data recorded from four

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different growth seasons, imposing higher night temperatures (reaching 29 oC), including a range

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of inbreds and hybrids tested under the same field-based tents. The data show no loss of spikelet

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fertility under HNT in field-grown rice (Fig. 3, Shi et al. 2013; Zhang Y et al. 2013). Therefore,

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we urge caution and awareness of the limitations when investigating HNT stress effects and


drawing conclusions from experiments carried out under controlled-environment conditions. One

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proposed strategy is to identify genetic resources that maintain a greater NSC pool in the stem

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and panicle and a higher biomass in spite of HNT to serve as good genetic donors to overcome

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HNT-induced yield losses. Predictions of significant damage that can be caused by a rapid

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increase in global night temperature indicate an urgent need to identify and validate a critical

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temperature threshold to facilitate thorough investigation of HNT-induced rice yield and grain

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quality losses under field conditions.

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Two recent reviews indicate the critical HDT thresholds for different growth stages of

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flooded rice crops (Shah et al. 2011; Sanchez et al. 2014). However, RH actually drives these

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thresholds under field conditions and this has been largely overlooked in many studies (see

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above reviews) and with regional or global estimates of heat stress (Gourdji et al. 2013; Teixeira

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et al. 2013), thus potentially overestimating the damage caused. The interaction between

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increasing temperature and the prevailing RH determines canopy temperature (Weerakoon et al.

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2008) and has been recently estimated in rice across multiple rice-growing regions of the world

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(Yoshimoto et al. 2011; Julia & Dingkuhn, 2013). These studies highlight a serious discrepancy

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in model estimations of damage when they neglect the effects of RH (White et al. 2011).

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Recently, two such studies modeled the impact of heat stress and spikelet sterility in rice

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(Nguyen et al. 2013; van Oort et al. 2014), with the former considering the flowering date of

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panicle and the time of day for anthesis, but considering only the air temperature. The latter

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study included panicle temperature, which accounts for the dynamics between temperature and

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RH, and also considered an arid and a humid climate. van Oort et al. 2014 showed that ignoring

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transpiration-cooling led to an overestimation of panicle sterility by 14 to 72%. Recent

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experimental and modeling efforts show that it is important to consider arid and humid


conditions in combination with higher temperatures for impact assessment studies and for

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strategic breeding efforts (Zhao & Fitzgerald, 2013).

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Another aspect of rice production that has received little emphasis is the impact of HDT

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or HNT (or a combination of both) on grain quality, which is equally important in terms of total

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economic returns, particularly in the whole-grain-consuming rice markets. Recently, the non-

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inclusion of grain quality in heat stress impact was shown to seriously underestimate milling

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outcomes, particularly head rice yield, and subsequent economic revenue (Lyman et al. 2013).

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Chalkiness is the major grain quality component that is increased by heat stress and hence is the

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focus of this section, although other aspects of grain quality such as moisture content, fissuring,

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cooking quality and palatability could be affected by higher temperatures (Fitzgerald et al. 2009;

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Fitzgerald & Resurreccion, 2009). Three routes are identified that could lead to increased chalk

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formation under heat stress: (i) source–sink relationship − lower source potential to meet sink

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demand or a reduction in grain-filling duration, which in both cases limits the availability or

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supply of sufficient assimilates for complete seed filling; (ii) starch metabolism enzymes in the

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sink; and (iii) hormonal imbalance, in particular the ratio of ABA and ethylene. High

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temperature during grain filling increases the rate of filling but the increase is found to be

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insufficient to compensate for the decrease in grain-filling duration (Kobata and Uemuki, 2004),

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resulting in increased chalkiness (Fitzgerald & Resurreccion, 2009). Similarly, under field

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conditions, rice exposed to HNT resulted in reduced NSC content of the panicles in a

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temperature-susceptible rice cultivar, leading to decreased grain width and increased chalkiness

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(Shi et al. 2013). Possible explanations are earlier degradation of the nuclear epidermal

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membrane, loose packaging of amyloplasts and poor water displacement from the gaps created

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by small and disorganized amyloplasts across both HDT and HNT (Ishimaru et al. 2009; Zakari


et al. 2002; Song et al. 2013). With a close association between grain filling and the availability

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of assimilates, the negative impact of increased dark respiration, particularly under HNT, leading

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to poor grain filling and quality can’t be ruled out. Attempts have been made to examine this

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aspect, but mostly using controlled-chamber conditions (Mohammed & Tarpley 2009a;

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Mohammed et al. 2013; Glaubitz et al. 2014). To date, there has not been a systematic analysis

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of HNT and the contribution of dark respiration to reducing NSC under realistic field conditions.

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This continues to be an intriguing hypothesis. The knowledge gap identified above is a major

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bottleneck preventing accurate quantification of the proportion of yield or quality loss that can be

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accounted for by dark respiration in the field.

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During grain filling, sugar supply may not be the only limiting factor, as starch

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metabolism enzymes such as sucrose synthase (SuSy), adenosine diphosphate glucose

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pyrophosphorylase (AGPase), starch synthase (StSase) and starch branching enzyme (SBE) are

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identified to be equally important in the successful conversion of sugars to starch (Yang &

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Zhang, 2010). Additionally, a high ABA-to-ethylene ratio is equally important during grain

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filling; external application of ABA has been shown to significantly stimulate grain filling

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(Zhang ZX et al. 2012). High temperature during grain filling is documented to reduce the

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expression of the sucrose transporter gene OsSUT1 and starch synthesis−related genes SuSy2,

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AGPS2b and BEIIb and granule-bound starch synthase in grains, with OsSUT1 reduced by about

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60% in the grains and flag-leaf tissue (Phan et al. 2013). A panicle clipping approach resulted in

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the up-regulation of OsSUT1 in response to increased assimilate supply, resulting in increased

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grain weight. A similar strategy employed by lowering planting density reduced yield losses in

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rice even under high temperature (Kobata & Uemuki, 2004), indicating a strong link between

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assimilate supply and enzymatic efficiency during grain filling. Contrasting views on the role of


α-amylase have been presented, with Hakata et al. (2012) recording a high negative correlation

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between chalky grains and α-amylase. They indicated that high temperatures induced activation

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of α-amylase as a crucial trigger for grain chalkiness. On the other hand, Ishimaru et al. (2010)

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proposed that changes in water distribution led to increased chalkiness under high temperature

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rather than starch degradation by α-amylase. A comprehensive atlas of the metabolomic and

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transcriptomic changes that occur during grain filling when exposed to high temperatures

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indicated either the down-regulation of sucrose import/degradation and starch biosynthesis or up-

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regulation of starch degradation to be the major bottleneck for efficient grain filling. The existing

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literature indicates an important role for starch metabolism (sugar transport and starch

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accumulation efficiency) in controlling chalkiness through sustained grain filling under high

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temperatures.

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Does pollen viability alone determine heat stress−induced spikelet sterility in rice?

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In response to increasing day temperatures, rice has three adaptive mechanisms, with one being

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heat avoidance through efficient transpiration-mediated cooling as highlighted above, and this is

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dependent on external factors. On the other hand, heat escape and true tolerance are inherent or

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can be genetically altered to increase adaptive resilience. Oryza species show a very wide

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variability in flowering time of day, for which some wild rice can flower as early as 6 AM (O.

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officinalis) or as late as 5 PM (O. australiensis), and a few can flower during the night (Sheehy et

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al. 2007). Most cultivated rice has its peak flowering occurring between 10 AM and 12 noon

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(Prasad et al. 2006). The phenomenon of early-morning flowering (EMF) has been exploited for

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the first time in rice (Ishimaru et al. 2010), wherein genetic alteration allows peak flowering to

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occur closer to dawn to help escape flowering from late-morning and early-afternoon heat.

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Although temperatures above the critical threshold occurring an hour after flowering have been


shown not to affect fertility (Jagadish et al. 2007), post-fertilization processes and early embryo

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growth can be potentially vulnerable under future warmer climates (Shi et al. 2014). Hence,

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options related to late-evening flowering (LEF) are another alternative strategy (Fig. 4), wherein

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the post-fertilization and early embryo formation phase would automatically occur under the

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much cooler night temperatures. Both EMF and LEF can only partially overcome heat damage as

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other sensitive developmental stages such as gametogenesis would still be equally vulnerable.

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An answer to the above would be to target true heat tolerance: the plants’ ability to set

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seed in spite of their peak flowering or other sensitive developmental stage coinciding with

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temperatures higher than the critical stress threshold, achieved by virtue of their resilient

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reproductive physiology. This resilience has been largely associated with pollen viability and the

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ability of pollen to germinate and fertilize. The role of the ovary is considered to be minimal

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based on cross-fertilization studies by Yoshida et al. (1981). In order to quantify the level of

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tolerance, both in vitro and in vivo pollen viability tests have been employed (Prasad et al. 2006;

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Jagadish et al. 2010). Using 25 diverse rice cultivars, pollen viability was estimated using pollen

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collected from the same set of plants, exposed to defined heat stress conditions (Fig. 5; Jagadish

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et al. UnPub). In vitro pollen viability estimated using an iodine starch stain (iodine potassium

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iodide) showed a poor correlation between pollen viability and spikelet fertility (r = 0.17) under

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control conditions and was even weaker (r=0.05) in response to heat stress (Fig. 5 A and B). On

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the other hand, using aniline blue to measure in vivo pollen viability by recording the percentage

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of pollen germination on the stigmatic surface resulted in a doubling of the correlation

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coefficient under control conditions (r = 0.34) and the correlation further increased in strength

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under heat stress (r = 0.68) (Fig. 5 C and D). Interestingly, the overall variability captured by in

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vivo pollen viability alone (R2 = 0.46, Fig 5 D) still left a lot of room for other aspects of pollen


development to be involved, such as pollen-tube growth rate (Jagadish et al. 2010), fertilization

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and early embryo abortion. The simple and fast iodine stain is frequently used to estimate in vitro

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pollen viability, but the poor correlation with fertility suggests that other techniques may be

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better suited to estimating pollen viability. Starch stains have been widely used as it is crucial

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that sufficient starch be available in the mature pollen to fuel subsequent fertilization events (De

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Storme & Geelen 2014). This allows the use of iodine stains to measure pollen viability.

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However, the role of pollen exine and intine, in particular the pollen coat, which comprises the

8

lipids and the proteins filling the exine cavities, is also essential for pollen viability (Suzuki et al.

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2008), and hence viability is not just determined by starch content. Recently, using sorghum

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(Sorghum bicolor) pollen, a significant reduction in phospholipids accompanied by an increase

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in reactive oxygen species accounted for a decrease in pollen activity under HNT (Vara Prasad &

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Djanaguiraman, 2011). Similar approaches targeting pollen lipid and protein compositional

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changes under heat stress conditions in contrasting rice cultivars would be an interesting future

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research direction. Progress achieved in this area would allow for a comparative analysis of

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pollen from diverse rice cultivars and other hardy species to identify mechanisms for heat

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tolerance and genetic markers to assist plant breeders. Such markers would be more robust than

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iodine stains and also less cumbersome than aniline blue staining, and could help establish a

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high-throughput phenotyping protocol to identify candidates with heat-tolerant pollen.

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The early developmental stages of pollen, including tetrad formation and early

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microspore stages, are also susceptible to heat stress (Jagadish et al. 2013). The impact of

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different abiotic stresses on early pollen development has been relatively well studied in

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sorghum and wheat (Jain et al. 2007, 2010; Ji et al. 2010, 2011; Oliver et al. 2007), but not in

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rice, except for Jagadish et al. (2013). Although a single study (Yoshida et al. 1981) indicates the


minimal role of the female reproductive organ in heat stress damage at anthesis, its vulnerability

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during the most sensitive gamete formation stage has not been tested. Many reviews highlight

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this as a challenge and a major knowledge gap in addressing abiotic stress−induced reproductive-

4

stage damage (Hedhly 2011; Hedhly et al. 2009).

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High temperature impact under future warmer climate

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Heat stress has been documented to have a negative interaction with drought and salinity stress

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(Mittler, 2006). In general, increased [CO2] concentration has a beneficial effect because of

8

increased photosynthesis (Shimono et al. 2013). However, increased biomass accumulation was

9

not effective in ameliorating the impact of HDT stress−induced spikelet sterility (Matsui et al.

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1997; Madan et al. 2012). Madan et al. (2012) tested three contrasting rice cultivars for high

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temperature and elevated CO2 combinations. The authors exposed the flowering stage to 5 days

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of heat stress while the plants were grown under elevated CO2 throughout the crop growth

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period. This experimental setup mimics a possible realistic scenario under gradually increasing

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atmospheric CO2 concentration accompanied by a predicted increase in frequency of short

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extreme heat spikes. None of the three cultivars benefited from elevated CO2 in terms of

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lowering spikelet sterility when temperatures exceeded the critical threshold. Hence, elevated

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CO2 is unable to compensate for heat stress damage during the flowering stage.

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The impact of heat stress under current and future warming scenarios (1 to 3 oC,

19

following IPCC, 2013) was mapped taking rice-growing regions of South Asia as a case study.

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Crop simulation models are increasingly being used to assess the impacts of climate change

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(Lobell & Gourdji, 2012). The amount of detailed information available will increase the

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accuracy of simulations that involve physiological processes. As an example, a complex

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simulation model that will track the diurnal variation of temperature will need hourly


temperature as an input. It is often impractical to use such a model for spatial impact studies as

2

the input requirement for such high-resolution data is not available. Hence, the most appropriate

3

simulation model should capture the summary effects of temperature on spikelet sterility by

4

using coarse-resolution data of climate variables at a daily time step. To explore the impact of

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future elevated temperature on spikelet sterility and its spatial variability, an upgraded version of

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rice crop growth simulation model ORYZA2000 (Bouman et al. 2001) that simulates growth at a

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daily time interval was used in our approach. The model simulates temperature responses to

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spikelet fertility according to Horie (1993). The relationship from Horie (1993) was derived

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across elevated and ambient CO2 concentrations and it shows that CO2 concentration has no

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10

effect on the temperature and spikelet fertility relationship (Bouman et al. 2001), similar to the

11

recent experimental evidence provided above. Using this model, we have explored the spatial

12

impact of elevated temperatures across rice-growing environments of South Asia.

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Standard input parameters describing crop growth and development were used as inputs

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to the model. A spatial soil dataset derived from the WISE soil database at 5 arc-minute

15

resolution (Batjes, 2006) was used as an input for the simulations. The simulations were carried

16

out on irrigated rice area grids having more than 75 hectares of rice area at 5 arc-minute

17

resolution using the MIRCA2000 database (Portmann et al. 2010). Daily solar radiation,

18

maximum and minimum temperatures, wind speed and vapor pressure from the NASA POWER

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dataset (http://power.larc.nasa.gov) were downscaled to 15 arc minutes and bias corrected

20

(Sparks, A. UnPub) and combined with daily rainfall data derived from Tropical Rainfall

21

Measurement Mission (TRIMM ) (http://trmm.gsfc.nasa.gov). The simulations were carried out

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under unlimited water and potential nitrogen supply for a 5-year period from 2006 to 2010 on the

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irrigated rice grids. The most recent IPCC report explores future climate change weather outputs


from several GCMs (Global Climate Models) and different representative concentration

2

pathways (RCPs). It is shown that RCP 8.5 in three GCMs predicts an increase in global mean

3

temperature (GMT) by 1 oC by the early 2020s, by 2 oC by the mid-2040s and by 3 oC by the

4

mid-2060s (Warszawski et al. 2013). Keeping this in mind, four different scenarios were created

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for simulations on irrigated rice grids across South Asia. A set of simulations with the original

6

weather (2006 to 2010) was the first scenario. An increase of 1 degree (scenario 2), 2 degrees

7

(scenario 3) and 3 degrees (scenario 4) centigrade to the daily maximum temperature represented

8

the other three scenarios. The CO2 fertilization effect was not considered. For all these scenarios

9

and for each rice grid, simulations were carried out once every 5 days during the planting

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window for the main rice season using a planting window database (IRRI, UnPub). From these

11

simulations, the best planting date was selected based on the average highest yields of five years

12

for each planting date for each grid from scenario 1. The five-year average spikelet sterility for

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the same planting dates from all the scenarios for each grid was chosen for the comparisons. The

14

percentage spikelet sterility in the simulations was calculated based on the number of spikelets

15

and number of grains.

16

Simulations under current weather quantify variability in spikelet sterility across the rice

17

grids (Fig. 6 and Table. 1). Some 39.5% of the rice area showed less than 5% spikelet sterility

18

and another 50% of the rice area has sterility ranging between 5 and 15% under the current

19

scenario (Fig 6A and Table 1). In general, sink size is in excess under potential conditions and up

20

to 30% of the spikelets could remain unfilled (Sheehy et al. 2001). Under scenario 2 (1 oC

21

increase), the area recording sterility between 5 and 15% increased to 62% (Table 1). The

22

percent area that recorded more than 30% sterility increased significantly with each degree

23

increase in temperature, i.e. 0.3% of the area under current conditions to as high as 24.4% with a


3-degree rise in temperature (Fig. 6 A and C; Table 1). Flowering in cultivated rice usually takes

2

place during the daytime. However, the time of day of flowering varies from early morning to

3

midday depending on the cultivar and environment as detailed earlier. The relationship built in

4

the model used was at best an approximation and a best possible representation to be used

5

regionally bearing in mind the available input data at this scale.

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6

Increasing temperature will affect several plant growth processes and spikelet sterility is

7

one of them. Among these effects, an increase in nighttime temperature is shown to decrease rice

8

yield (Peng et al. 2004; Welch et al. 2010). Currently, few models have the capability to simulate

9

the effects of increased temperature on different crop growth and development processes.

10

ORYZA2000 is one of the few that has a temperature response function to simulate spikelet

11

sterility. However, other aspects such as response to increased minimum temperature and the

12

interactions of increased temperature and RH (vapor pressure difference) need to be addressed to

13

reduce uncertainties in simulating future impacts of climate change. Process-based understanding

14

of these issues is a precursor to incorporating such functionalities into simulation models.

15

Conclusions and future perspectives

16

Solutions to overcome current challenges faced with increasing temperature-induced yield losses

17

have advanced significantly, but examining the complex issues surrounding grain quality losses

18

continues to be a major challenge. Additional challenges that could emerge with the transition

19

from fully flooded rice cultivation to water-saving technologies need greater emphasis to ensure

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that the advantage gained under fully flooded conditions facilitates the transition with minimum

21

damage under a future warmer and drier climate. To ensure sustained adoption of water-saving

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technologies under future hotter climates, rice cultivars with enhanced tolerance of heat and

23

combined heat and drought stress during the floral meristem stage will be crucial to complement


the progress achieved in overcoming the damage across other sensitive developmental stages

2

such as flowering. With a more recent increase in research interest in addressing HNT impacts

3

on rice, caution needs to be exercised in imposing the right levels of stress and targeting traits

4

that can overcome the damage under realistic field conditions. In addition, the dynamic change in

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temperature amplitude due to differential day and night temperature increase could potentially

6

affect crops differently than the known mechanisms of damage induced by either HDT or HNT.

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The emergence of tolerant cultivars such as N22, which can tolerate both HDT and HNT at

8

flowering and gametogenesis stages, and heat-escaping strategy by employing EMF or LEF,

9

provides excellent opportunities to breed heat escape, tolerance or a combination of both

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strategies to induce greater resilience in rice to increasing temperatures. The quest to identify

11

such novel donors that can tolerate heat stress across sensitive developmental stages and

12

different environmental conditions needs to be intensified to provide sufficient options to

13

mitigate the impact of heat stress across hot-dry and hot-humid locations. In principle, the rice-

14

growing areas currently in the hot-dry regions with an advantage from transpiration cooling

15

could well be much more greatly affected than hot-humid regions with reduced irrigation

16

availability or the transition to water-saving technologies. To overcome damage at the flowering

17

stage, phenotyping protocols have been standardized for quantifying pollen viability, but a more

18

reliable and high-throughput technique or markers that can potentially allow assessment of large

19

genetic panels have yet to be identified. In comparison to the impact of heat stress on yield, the

20

mechanism leading to grain quality losses is more complex and requires intensified efforts to

21

continue producing high-quality grain. An interesting relationship between altered assimilate

22

supply and the expression of starch metabolic enzymes opens up an opportunity to identify

23

mechanisms regulating panicle senescence that could extend grain-filling duration. A high-


throughput technique such as chlorophyll fluorescence imaging that could quantify the active

2

grain-filling duration would be a way to identify new germplasm with longer grain-filling

3

duration under stress. This extension of grain-filling duration would help counteract the direct

4

impact of heat stress and indirectly postpone the enzymatic trigger that stops active starch

5

metabolism in filling grains. Interestingly, the critical role of sugars/carbohydrates and invertases

6

in overcoming the negative impact of abiotic stress (cold, drought and heat stress) during

7

gametogenesis and early pollen development has been documented across cereals (Ji et al. 2010;

8

Jain et al. 2010; Nguyen et al. 2010). On the other hand, a higher CO2 resulting in increased

9

biomass and assimilate supply fails to reduce heat stress−induced spikelet sterility losses at the

10

anthesis stage (Madan et al. 2012), indicating a missing link to stress response in reproductive

11

organs across their developmental stages. Finally, the major factor driving climate change is

12

increased CO2 and it is projected to continue to increase gradually, but research indicates a lack

13

of amelioration of heat stress−induced yield loss under elevated CO2 conditions. However,

14

progress achieved through breeding efforts to safeguard sensitive reproductive processes from

15

heat stress would allow better use of the additional biomass accumulated from gradually

16

increasing [CO2]. Indeed, this is an intriguing hypothesis that could partially address the

17

persisting challenge to increase rice productivity in spite of a projected warming climate.

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Accepted Article

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Accepted Article

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Peng S., Huang J., Sheehy J.E., Laza R.C., Visperas R.M., Zhong X., …, Cassman K.G. (2004) Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America 101, 9971−9975.

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Shi W., Ishimaru T., Gannaban R.B., Oane W. & Jagadish S.V.K. (2014) Popular rice (Oryza sativa L.) cultivars show contrasting responses to heat stress at gametogenesis and anthesis. Crop Science doi:10.2135/cropsci2014.01.0054.

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Figure legends

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Fig. 1 Rice plants maintained under fully flooded conditions exposed to control (30 oC) and heat

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stress (39 oC) for consecutive 4 days (6 hours of stress [0900 to 1500] on each day following

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Jagadish et al. 2010) coinciding with the panicle initiation stage resulted in no reduction in

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spikelet fertility (A) or sink size (B). Grey striped bars are data obtained from independent

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experiments and data for number of spikelets in N22 (6264) is not available. Numbers in

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parentheses after the cultivar are the IRRI Genebank accession numbers. Bars indicate ±SE

9

(Jagadish et al. UnPub).

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Fig. 2 Soil, water and air temperature recorded using thermocouples under control (30 oC) and

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high temperatures (39 oC) for consecutive 4 days (6 hours of stress [0900 to 1500] on each day

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following Jagadish et al. 2010) coinciding with panicle initiation stage under fully flooded pots

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in controlled environment chambers (A). Soil, air and panicle temperature under fully flooded

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(puddled) transplanted rice (PTR) and direct-seeded rice (DSR) at 10 kPa (B), recorded using

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water-proof temperature pendants (Onset HOBO data loggers, Utah, USA) for 15 days

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coinciding with flowering. Panicle temperature on ten independent panicles was recorded under

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PTR and 10 kPa DSR conditions using a thermal camera (NEC Avio Infrared Technologies Co.

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Ltd., Tokyo, Japan). Bars indicate SE.

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Fig. 3 High night temperature (HNT) exposure under controlled environments (A) and field

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conditions (B) shows contrasting responses to stress impact on spikelet fertility, with only the

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former recording a significant decline in fertility. Published literature using environmentally

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controlled growth chambers (control night temperature ranging between 22 and 27 oC and HNT

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from 30 to 32 oC − Mohammed and Tarpley, 2011 and 2010; Cheng et al. 2009; Mohammed et

24

al. 2013) indicates HNT inducing a significant reduction in spikelet fertility. Under field 32

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conditions (see supplementary Fig. S1 in Shi et al. 2013), exposure to optimum night

2

temperature between 22 and 23 oC and HNT ranging between 28 and 29 oC using two contrasting

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cultivars (Shi et al. 2013) from a preliminary screen of 36 cultivars over four different seasons

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exposed to day/night temperature of 22/27 oC (Zhang Y et al. 2013) indicated no reduction in

5

spikelet fertility. Similarly, diverse genotypes, across four seasons (two dry seasons (DS) and

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two wet seasons (WS) at IRRI), involving HNT and different nitrogen levels (150 and 250 N

7

during the DS and 75 and 125 N during the WS) and interactions (Shi et al. UnPub. data

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indicated by blue and white bars in panel B), including different indica cultivars and hybrids,

9

validate the hypothesis that HNT does not directly lead to a yield reduction through a decline in

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spikelet fertility. Average day temperatures across all the field experiments including Zhang Y et

11

al. (2013) and Shi et al. (2013) varied between 27 and 30 oC. Day temperatures ranged between

12

32 and 33.9 oC in Cheng et al. (2009) and Mohammed and Tarpley (2013), with Mohammed and

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Tarpley 2010 and 2011 recording temperatures ranging between 31.6 and 32.8 oC.

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Fig. 4 Time of day of flowering as an adaptive mechanism to mitigate high-temperature-induced

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reduction in spikelet fertility. Data presented for Oryza sativa Koshihikari and Koshihikari early-

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morning flowering (EMF) line were extracted from Ishimaru et al. (2010). The flowering pattern

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of O. australiensis indicating the late-evening flowering (LEF) was obtained by recording the

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flowering pattern over 5 flowering days (Quinones et al. UnPub) and supports the finding of

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Sheehy et al. (2007).

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Fig. 5 Pollen viability estimated using iodine potassium iodide (IKI) correlates poorly with

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spikelet fertility under control (A; Y=0.43x + 43.42, R2=0.03, n = 31 entries) and more so under

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heat stress (B; Y=0.02x + 84.93, R2=0.003, n=31). In vivo pollen viability measured by number

23

of pollen germinated on the stigma is strongly correlated with spikelet fertility under control (C;


Y=0.22x + 83.51, R2=0.12, n=32) and with higher significance under heat stress (D; Y=0.23x +

2

2.15, R2=0.46, n=32). Black circles (Jagadish et al. UnPub) are data obtained simultaneously

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from the same set of plants following the same crop management practices and exposed to 39 oC

4

following Jagadish et al. (2010) and white circles are data extracted from published literature

5

(Prasad et al. 2006; Rang et al. 2011; Jagadish et al. 2010).

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Fig. 6 Spatial variability of percent spikelet sterility across South Asia with current (2006 to

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2010) temperature as baseline (A), and , 2 oC (B) and 3 oC (C) increase in maximum

8

temperature.

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Table 1 Percent rice area across South Asia and spikelet sterility induced under current and three

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future scenarios, that is with 1, 2 and 3 oC increase in maximum temperature over the current

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baseline (2006 to 2010) and coinciding with the critical flowering stage. Numbers in the table

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indicate percent rice area.

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Temperature

Spikelet sterility (%)

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