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Keeping a cool head: gene networks underlying chilling-induced male sterility in rice1 Graham Noctor Institut de Plant Sciences Paris-Saclay, Université Paris-Saclay, 91405 Orsay cedex, France

Tel : 33(0)169153301 e-mail : [email protected]

Submitted as a commentary on: Cooling water before panicle initiation increases chilling-induced male sterility and disables chillinginduced expression of genes encoding OsFKBP65 and heat shock proteins in rice spikelets. Suzuki et al.

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.12513 This article is protected by copyright. All rights reserved.

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Over the last two decades, research on redox processes has outgrown the once narrower primary focus on biological energy transduction. We now know that as well as driving the engine that underpins plant growth, redox reactions feed information into signalling circuits and intermesh intimately with phytohormone functions. Stress signals are transmitted, at least in part, by changes in redox state, allowing reactive oxygen species (ROS), nitric oxide, and related molecules to form a crucial interface between the development of plants and their fluctuating, imperfectly predictable environment. As climate is forecast to include more extreme events in the coming decades, understanding redox-related signalling will become ever more important to efforts to apply the basic knowledge of plant science to crop performance in the field (Munné-Bosch et al. 2013). It is still far from clear how ROS and other redox-active molecules influence various developmental processes in plants. In this issue of Plant, Cell & Environment, Suzuki et al. (2015) report a transcriptomics-based analysis of factors underlying chilling-induced male sterility in rice, one of the world’s most important crops. As a plant of sub-tropical origin, rice is susceptible to cool temperatures: pollen production during anther development is particularly sensitive. At this critical stage, even slight cooling (temperatures as high as 18-20°C) can cause degeneration of a significant proportion of the developing pollen grains in some varieties. The underlying mechanisms are imperfectly described, but previous studies have implicated hormones such as abscisic acid (ABA; Oliver et al. 2007). Beginning from the observation that sterility caused by exposing young anthers to chilling temperatures is exacerbated if plants have been pre-exposed to cooler temperatures during vegetative growth (Shimono et al. 2012), the authors describe gene expression patterns associated with this effect (Suzuki et al. 2015). The use of a three-way comparison enabled the effect of precooling on the chill response to be compared with effects of pre-cooling and chilling in themselves, generating a complex and potentially informative set of data (Fig. 1a). One effect that emerges clearly is that pre-cooling antagonizes the up-regulation of core stress response systems by subsequent chilling. Systems most obviously affected in this way include genes encoding various antioxidative enzymes and different types of heat-shock proteins (HSPs) as well as certain heat-shock factors (HSFs). Together with earlier transcriptomic studies of the heat sensitivity of tomato pollen production (Frank et al. 2009), the study further documents the key role of ROS homeostasis at the hub of physiological and developmental responses to sub-optimal conditions. However, the study of Suzuki et al. (2015) raises several interesting additional points. First, the cooling-induced loss of part of the chilling response contrasts with the acclimation model, according to which pre-exposure generally mitigates the effects of a subsequent stress episode. Further, exactly how cool temperatures perceived during the vegetative stage affect responses at the reproductive stage raises issues of both “memory” and of systemic signalling, hot topics in research on ROS and temperature stress (Miller et al. 2009; Wu et al. 2013). Another interesting point concerns the networks that interact with the ROS-related components in determining chilling-induced male sterility. The data confirm the involvement of the key stress hormone, ABA, and of heat-shock components in temperature responses. While the exact functions of many of these components are not yet established, both HSPs and certain HSFs are involved in responses to ROS at some level (Miller & Mittler 2006). Specific HSFs may be important in regulating ROS-induced gene expression, while the various classes of plant HSPs can promote protein stability in the face of increased oxidation. In addition, some HSPs are involved in delivering proteins for

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degradation by the ubiquitin-dependent proteasome pathway. As well as allowing removal of “damaged” proteins, proteasome activity is required to promote signalling pathways by targeted degradation of repressor proteins. Such repressors include the class VII group of ethylene response transcription factors (ERFs) involved in oxygen and nitric oxide sensing in Arabidopsis (Gibbs et al. 2014).

In contrast to recent advances in the field of oxygen sensing, and despite close scrutiny of ROSinduced transcriptomes, “ROS sensors” remain elusive. Intriguingly, networks involved in anoxia sensing have been shown to overlap considerably with those that mediate heat stress responses, with low oxygen inducing several HSPs and HSFs (Banti et al. 2010). Indeed, a gene encoding pyruvate decarboxylase, an enzyme that can promote fermentation when respiration is oxygenlimited, was affected by pre-cooling in a similar way to antioxidative enzymes and HSPs (Suzuki et al. 2015). In deepwater varieties of rice, low internal oxygen caused by submergence provokes an important stem elongation response mediated by ethylene-dependent expression of ERFs that then trigger very rapid gibberellin (GA)-dependent internode growth (Hattori et al. 2009). A number of ERFs were among genes most obviously down-regulated by pre-cooling, along with several E3ubiquitin protein ligases, which confer specificity in ubiquitination and, therefore, proteolysis. It is well documented that mutations in GA synthesis or signalling were responsible for the development of the shorter “green revolution” varieties of rice and other cereals that are dominant in contemporary agriculture (Peng et al. 1999; Sasaki et al. 2002). As well as stem elongation, GAs are required both for pollen production and pollen tube growth (Aya et al. 2009). Another recent study clearly implicates compromised GA signalling in the sensitivity of pollen production to cool temperatures. Not only was the expression of certain GA synthesis and signalling genes altered in young anthers subjected to cooling, but the decrease in pollen production was exacerbated in GAdeficient or GA-insensitive rice and rescued by exogenous GA (Sakata et al. 2014). Like oxygen sensing, cellular perception of GAs depends on controlled, proteasomal degradation of repressors (DELLA proteins) that have been implicated in ROS-related stress responses in plants (Achard et al. 2008). Interestingly, a recent analysis of DELLA interactants identified members of the class VII ERF transcription factors known to be involved in oxygen sensing (Marín-de la Rosa et al. 2014). Based on these and other recent developments, it is tempting to speculate that temperature variations during the vegetative and reproductive phases of rice cultivation impact male fertility through ROS-linked redox regulation of GA-ABA networks, and that certain ERFs and HSPs play central roles in these interactions (Fig. 1b).

The data-rich study of Suzuki et al. identifies other interesting transcriptomic patterns. These include effects on gene expression associated with jasmonic acid, another hormone that is known to be crucial in male fertility (Xie et al. 1998). Significant changes in secondary metabolism and pathogenesis-related genes further highlight the overlap between responses to biotic and abiotic stresses. The findings join many others in underscoring the intricate links between ROS and phytohormone pathways, showing both that redox modifications can strongly impact hormone action and that ROS signalling largely acts by interacting with these pathways. Other studies will be required to test the functional importance of the transcriptomic changes, but the work opens up several interesting avenues relating to the regulatory mechanisms that underlie an agronomically important problem. It should stimulate even more scrutiny of redox-dependent signalling, an

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intensively studied area whose relevance to crop performance in challenging conditions is unlikely to diminish in the near future. Acknowledgments The author would like to acknowledge the authoritative input and constructive suggestions of two referees during review of the article by Suzuki et al. (2015).

References

Achard, P., Renou, J.P., Berthomé, R., Harberd, N.P. & Genschik, P. (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biology 18, 656-60. Aya, K., Ueguchi-Tanaka, M., Kondo, M., Hamada, K., Yano, K., Nishimura, M. & Matsuoka, M. (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. The Plant Cell 21, 1453–1472. Banti, V., Mafessoni, F., Loreti, E., Alpi, A. & Perata, P. (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiology 152, 1471–1483. Frank, G., Pressman, E., Ophir, R., Althan, L., Shaked, R., Freedman, M., Shen, S. & Firon, N. (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. Journal of Experimental Botany 60, 3891-3898. Gibbs, D.J., Bacardit, J., Bachmair, A. & Holdsworth, M.J. (2014) The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions. Trends in Cell Biology 24, 603-611. Hattori, Y., Nagai, K., Furukawa, S., Song, X.J., Kawano, R., Sakakibara, H., Wu, J., Matsumoto, T., Yoshimura, A., Kitano, H., Matsuoka, M. & Ashikari, M. (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026–1030.

Marín-de la Rosa, N., Sotillo, B., Miskolczi, P., Gibbs, D.J., Vicente, J., Carbonero, P., Oñate-Sánchez, L., Holdsworth, M.J., Bhalerao, R., Alabadí, D. & Blázquez, M.A. (2014) Large-scale identification of gibberellin-related transcription factors defines group VII ETHYLENE RESPONSE FACTORS as functional DELLA partners. Plant Physiology 166, 1022-1032. Miller, G., Mittler, R. (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Annals of Botany 98, 279–288.

Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M.A., Shulaev, V., Dangl, J.L. & Mittler, R. (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45.

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Munné-Bosch, S., Queval, G. & Foyer, C.H. (2011) The impact of global change factors on redox signaling. Plant Physiology 161, 5-19. Oliver S.N., Dennis E.S. & Dolferus R. (2007) ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant and Cell Physiology 48, 1319-1330. Peng, J., Richards, D.E., Hartley, N.M., Murphy, G.P., Devos, K.M., Flintham, J.E., Beales, J., Fish, L.J., Worland, A.J., Pelica, F., Sudhakar, D., Christou, P., Snape, J.W., Gale, M.D. & Harberd, N.P. (1999) 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400, 256-261.

Sasaki, A., Ashikari, M., Ueguchi-Tanaka, M., Itoh, H., Nishimura, A., Swapan, D., Ishiyama, K., Saito, T., Kobayashi, M., Khush, G.S., Kitano, H. & Matsuoka, M. (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416, 701-702.

Sakata T., Oda S., Tsunaga Y., Shomura H., Kawagishi-Kobayashi M., Aya K., Saeki, K., Endo, T., Nagano, K., Kojima, M., Sakakibara, H., Watanabe, M., Matsuoka, M. & Higashitani A. (2014) Reduction of gibberellin by low temperature disrupts pollen development in rice. Plant Physiology, 164, 2011–2019 Shimono H., Suto M. & Nagano K. (2012) Cold tolerance for sterility induced by low temperature at booting stage can be improved by warmer water temperature during vegetative growth. Climate in Biosphere 12, 1-5. Suzuki, K., Aoki, N., Matsumura, H., Okamura, M., Ohsugi, R. & Shimono, H. (2015) Cooling water before panicle initiation increases chilling-induced male sterility and disables chilling-induced expression of genes encoding OsFKBP65 and heat shock proteins in rice spikelets. Plant, Cell & Environment (this issue) Wu, T.Y., Juan, Y.T., Hsu, Y.H., Wu, S.H., Liao, H.T., Fung, R.W.M. & Charng, Y.Y. (2013) Interplay between heat shock proteins HSP101 and HSA32 prolongs heat acclimation memory posttranscriptionally in Arabidopsis. Plant Physiology 161, 2075-2084. Xie, D.X., Feys, B.F., James, S., Nieto-Rostro, M. & Turner, J.G. (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094.

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Figure legend Figure 1. Interactions between temperatures during the vegetative and reproductive stages of rice in determining pollen fertility. (a) Three-way comparison of transcriptomes to explore processes underlying effects of pre-cooling on the chill response in rice anthers (Suzuki et al. 2015). (b) Hypothetical scheme showing how some of the factors identified in this study might be interacting. Chilling during anther development negatively affects pollen production, despite inducing a number of defensive responses that mitigate this effect by promoting cellular homeostasis or by maintaining appropriate signalling (represented by the red figure in the top half of the cartoon pushing back against the stress). Pre-cooling at the vegetative stage somehow weakens this stabilizing part of response to chilling, leading to more marked effects on male sterility (lower half of cartoon). While the links between temperature perception during the two stages of development remain unclear, phytohormones or ROS levels may be involved. ABA, abscisic acid. GA, gibberellins. HSP, heat-shock protein. ROS, reactive oxygen species.

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(a)

Figure 1

(b)

Vegetative stage

Spikelets

Cooled

Chilled

Noncooled

Chilled

Noncooled

Nonchilled

Cooled

Nonchilled

Vegetative stage

Effect of cooling on chill response Chill response Cooling response

Spikelets Pollen production

Chill

Optimal temperature

Antioxidants HSPs GA signalling

Ethylene?

Cool temperature

ABA? Systemic ROS?

Pollen production

Chill Antioxidants HSPs GA signalling

Keeping a cool head: gene networks underlying chilling-induced male sterility in rice.

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