Physiological mechanism underlying spikelet degeneration in rice

Key Laboratory of Crop Genetics and Physiology of Jiangsu Province/Innovation Center for Modern Production Technology of Grain Crops of Jiangsu Province, Yangzhou University, Yangzhou 225009, P.R.China

1. Introduction

Grain yield of rice (Oryza sativa L.) is determined by four components: panicle number per unit area, spikelet number per panicle, seed-setting rate or filled grain percentage,and grain weight. Among the four components, panicle number per unit area is constrained by space conditions and exists a certain degree of saturation; grain weight or 1 000-grain weight is more controlled by genetic factors and shows relative stability for a cultivar; filled grain percentage is determined not only by water and nutrient supply but also by temperature and light conditions during maturity; while spikelet number per panicle has great potential of increases,due to its large variability and adjustability, and its increase has always been a main approach to achieve a higher grain yield in both breeding and culture (Yang and Zhang 2010; Wang 2011; Vriet et al. 2012; Gonzalez-Navarro et al.2015). The number of spikelet per panicle depends not only on the number of differentiated spikelets, but also on the degeneration rate of spikelets. In general, the number of degenerated spikelets accounts for 15–20% of the total differentiated spikelets. The spikelet degeneration rate can be 50–60% for some cultivars or under the unfavorable conditions such as high temperature or drought during and/or around meiosis (Matsushima 1980; Tan et al. 2011; Xie et al. 2013; Zhang C X et al. 2017; Zhang W Y et al. 2017;Zhang 2018).

The development of a young rice panicle can be divided into two main stages: the first stage is from panicle initiation(the neck-node differentiation stage) to the end of spikelet primordium differentiation, in which primary and secondary branches and spikelets are differentiated; and the second stage is from pistil and stamen differentiation to the heading stage. The elongation of branches and spikelets, formation of floral organs, meiosis, and the filling of pollen grains are completed, and spikelet degeneration also happens during this period (Matsushima 1980; Itoh et al. 2005).According to the degeneration time and position on a panicle,spikelet degeneration can be divided into two types: spikelet degeneration (preflowering floret abortion) and spikelet barrenness (Matsushima 1980; Itoh et al. 2005; Li et al.2009). Spikelet degeneration, including the degeneration of either some spikelets or all spikelets on a branch (branch degeneration), mainly occurs on the proximal branches of a panicle and during meiosis or at the base part of panicle in early young panicle development. In contrast, spikelet barrenness mainly happens on the distal branches of a panicle and from the filling of pollens to the heading or at the top of panicle in late young panicle development. The proportion of the two kinds of spikelet degeneration varies with rice cultivars and the conditions of panicle development. It is observed, however, that some modern rice cultivars that have numerous spikelets on a panicle have shown more spikelet barrenness (Itoh et al. 2005; Li et al. 2009; Tan et al. 2011;Wang et al. 2012). Either spikelet degeneration or spikelet barrenness can result in a substantial decrease in spikelet number, and consequently, a serious loss of grain yield (Tan et al. 2011; Wang et al. 2012; Zheng et al. 2014, 2016; Zhang C X et al. 2017; Zhang W Y et al. 2017; Zhang 2018).

Spikelet degeneration occurs not only in rice, but also in other cereal crops such as wheat (Triticum aestivum L.) and maize (Zea mays L.) although the structure of inflorescence of spikelet among these crops is different. There are reports showing that 160–180 florets can usually be differentiated on a wheat spike, but approximately 70% of them could be degenerated, and in maize, floret degeneration or seed abortion rate could be as high as 30–50% (Wang 2011; Xie et al. 2013). Why do these crops degenerate so many spikelets or florets? Understanding the mechanism in which spikelet/floret degeneration occurs would have great significance in enhancing yield potential in cereals.

Therefore, taking rice as an example, the paper reviewed the physiological mechanism underlying spikelet degeneration,with focus on the roles of phytohormones in regulating the process.

2. Explanations for spikelet degeneration

2.1. Resource limitation

For a long time, the mechanism of spikelet degeneration in crops has been studied from different perspectives, and various explanations or hypotheses have been put forward(Matsushima 1980; Patel and Mohapatra 1992; Wang 2011).Among them, resource limitation is a classic assumption.It is proposed that spikelet degeneration in rice is mainly resulted from the constraint of resource or nutrient supply,and under such conditions, some late differentiated spikelets are at a disadvantage in competition for and could not get enough nutrients, leading to degeneration (Cock and Yoshida 1972; Singh and Jenner 1982; Ishimaru et al. 2005;Kamoi et al. 2008). There is a report showing that ozone stress inhibited rice spikelet differentiation and promoted spikelet degeneration, which was closely associated with decreased accumulation of nitrogen (N) and biomass during the panicle development (Wang et al. 2012). There are many reports, however, that serious degeneration of spikelets still happens even under the good condition of nutrient supply (Mohapatra et al. 1993; Afza et al. 2000;Xie et al. 2013; Zhang W Y et al. 2017; Zhang 2018). It is observed that spikelet degeneration in rice subjected to soil drying during the booting stage occurs neither by reduced assimilation nor by water deficits in the shoot, but by some chemical signals from roots to shoots (Kobata et al. 1994).These results imply that resource limitation only accounts partly for spikelet degeneration.

2.2. Self-organization

It is hypothesized that spikelet or floret degeneration in plants is a self-organized process, that is, the random migration of initial resources results in the imbalance of resource allocation among the developmental sinks, and this initial imbalance expands and forms the dominant level for the superior sinks that obtain more resources through autocatalytic process, which leads to the degeneration of inferior sinks that could not get enough resources(Caneshaiah and Uma 1994). Actually, however, spikelet degeneration in most cereals is not randomly. For example,spikelet degeneration happens at the base and the top of a rice panicle. In wheat, floret degeneration occurs at the distal position in a spikelet or at both base and top of a spike.Kernel abortion is mainly at the top of an ear in maize. These characteristics of spikelet or floret degeneration in cereals could not support the hypothesis of “random migration of initial resourcesself-organization processinferior sink degeneration”.

2.3. Roles of phytohormones in regulating spikelet degeneration

Five classic phytohormonesIt is generally believed that plant hormones are key regulators to seed development, and the roles of five classic plant hormones, auxins, cytokinins,gibberellins (GAs), abscisic acid (ABA), and ethylene, in regulating spikelet differentiation and degeneration have been documented (Brenner and Cheikh 1995; Yang et al.2001; Davies 2004; Pandey 2017). It is generally assumed that spikelet degeneration is a result of apical dominance or primigenic dominance (Bangerth 1989). In the hypothesis of primigenic dominance, indole-3-acetic acid (IAA) export of the earlier developed sink is suggested to inhibit the IAA export of later developed sinks, and this depressed IAA-export of the subordinated fruit/sink acts as the signal that leads to inhibited development, and consequently, fruit or sink degeneration (Bangerth 1989; Finkelstein 2004).Using a mutant, aberrant spikelets and panicle1 (asp1), that exhibits disorganized branching patterns and phyllotaxy,abnormal morphology of spikelets and rachis, premature termination of spikelet development, and reduced numbers of mature spikelets and branches. Yoshida et al. (2012) have observed that ASP1 encodes a transcriptional co-repressor similar to Arabidopsis TOPLESS and TOPLESS RELATED genes, and auxin signaling and histone deacetylase action contribute partially to defective in the mutant. However,there are reports showing that the difference in IAA concentration in spikelets at different positions on a rice panicle is very small before ovaries are pollinated (Patel and Mohapatra 1992; Duan et al. 1999; Pandey 2017). Drought during meiosis significantly increased spikelet degeneration but IAA concentration was not significantly decreased in rice panicles (Yang et al. 2008). The spray of IAA could not alleviate spikelet degeneration when rice was grown under saline flooding conditions (Yokoyama et al. 2002).Moreover, spikelets on the top of a rice panicle that have higher concentration of IAA could also degenerate (Itoh et al.2005; Li et al. 2009; Tan et al. 2011). These results may be difficult to back the hypothesis that apical dominance causes floret degeneration.

Apart from IAA, cytokinins and GAs are considered as other two kinds of promoting phytohormones because they can generally enhance plant growth and development(Morris et al. 1993; Brenner and Cheikh 1995; Davies 2004;Pandey 2017). It is observed that application of GA3could suppress spikelet degeneration when rice subjected to saline flooding (Yokoyama et al. 2002) and pre-anthesis spraying 6-benzylaminopurine decreased floret degeneration rate in wheat (Zheng et al. 2014, 2016). However, other studies show that levels of GAs and zeatin+zeatin riboside (Z+ZR)in young rice panicles are not decreased although spikelet degeneration rate was significantly increased when the plants subjected to drought during meiosis (Yang et al.2008), and applying kinetin to rice plants could not decrease the spikelet degeneration caused by saline irrigation(Yokoyama et al. 2002).

In contrast to IAA, cytokinins, and GAs, both ethylene and ABA are generally regarded as inhibitory growth regulators(Trewavas and Jones 1991; Beltrano et al. 1994; Cheng and Lur 1996; Mohapatra et al. 2000; Yang et al. 2006a). A high ethylene evolution rate has frequently been related to floret degeneration or seed abortion in maize (Cheng and Lur 1996) and wheat (Xu et al. 1995; Beltrano et al. 1999),and spikelet degeneration in rice (Yang et al. 2006b, 2007a,2008). There is a report showing that the anthers located on the distal floret positions of a wheat spikelet contain higher ABA levels than those on the proximal positions, and the high ABA concentration is linked to the reduced grain set(Lee et al. 1988). Under water stress, an increase in floret abortion in wheat has been observed to be associated with an elevated level of ABA florets (Saini and Aspinall 1982;Ahmadi and Baker 1999). However, the work of Yang et al.(2007a, 2008) has shown that both ABA and ethylene are all enhanced in rice spikelets by water stress imposed during meiosis, but ethylene is enhanced more than ABA in a rice cultivar with a higher rate of spikelet degeneration when compared with a cultivar with a lower rate of spikelet degeneration. They observed that spikelet degeneration was significantly reduced when ABA or aminoethoxyvinylglycine(AVG), an inhibitor of ethylene synthesis, was applied to water-stressed panicles at the early meiosis stage, and application of ethephon, an ethylene-releasing agent, or fluridone, an inhibitor of ABA synthesis, had the opposite effect, and the spikelet degeneration rate was increased.It is argued that antagonistic interactions between ABA and ethylene may be involved in mediating the effect of water stress on spikelet degeneration. A higher ratio of ABA to ethylene would be a physiological trait of rice adaptation to water stress (Yang et al. 2007a, 2008).

New phytohormones of brassinosteroids (BRs) and polyamines (PAs)Both BRs and PAs are two types of important new phytohormones (Davies 2004; Wu et al.2008; Hou et al. 2013; Pandey 2017). It is believed that BRs are a group of naturally occurring novel plant steroid hormones comprising brassinolide, castasterone, and their various derivatives that play critical roles in a wide range of plant developmental processes including seed germination, vascular differentiation, pollen tube growth,nucleic acids and protein biosynthesis, and the production of flowers and fruit by producing an array of physiological changes (Jiang et al. 2013; Vriet et al. 2013; Zhao et al.2013; Fariduddin et al. 2014). There is a study showing that concentrations of 24-epicastasterone (24-epiCS) and 28-homobrassinolide (28-homoBL) in young rice panicles from panicle initiation to pollen mother cell meiosis were significantly and positively correlated with the number of spikelet differentiation, while significantly and negatively correlated with the percentage of spikelet degeneration(Zhang 2018). Changes in the levels of antioxidant system(AOS), proton-pumping ATPase activity, ATP concentration,and energy charge were consistent with the changes in 24-epiCS and 28-homoBL concentrations. The contents of hydrogen peroxide (H2O2) and malondialdehyde (MDA) were opposite to the levels of 24-epiCS and 28-homoBL (Zhang 2018). Application of 24-epiCS or 28-homoBL to young panicles markedly increased the concentrations of 24-epiCS or 28-homoBL in the panicles, energy charge, AOS levels and spikelet differentiation, whereas significantly decreased the contents of H2O2and MDA and spikelet degeneration.The opposite effects were observed when an inhibitor of brassinosteroids biosynthesis, brassinazole, was applied(Zhang 2018). The results indicate that BRs play a vital role in promoting spikelet differentiation and supressing spikelet degeneration though enhancing AOS and energy charge during the panicle development period of rice.

PAs are well known to play important roles in many physiological processes, including cell division,morphogenesis, embryogenesis, fruit set and growth,senescence, and responses to environmental stresses(Yang et al. 2007b; Alcazar et al. 2010; Nambeesan et al.2012; Chen et al. 2013; Zhang W Y et al. 2017). The recent work of Zhang W Y et al. (2017) has shown that a moderate soil-drying (MD) treatment imposed from the onset of panicle initiation to the pollen completion stage could significantly increase spikelet differentiation and decrease spikelet degeneration compared to the well-watered treatment. The increase in spikelet differentiation and decrease in spikelet degeneration are closely associated with increases in contents of free spermidine (Spd), free spermine (Spm), the ratio of free putrescine (Put), and free-Spd or free-Spm to 1-aminocylopropane-1-carboxylic acid (ACC). When Spd or AVG, an inhibitor of ethylene synthesis, was applied to young panicles, the Spd and Spm contents and spikelet differentiation were increased, whereas ACC contents and spikelet degeneration were decreased significantly. The results were reversed when ACC or methylglyoxal-bis(guanylhydrazone), an inhibitor of Spd and Spm synthesis,was applied (Zhang W Y et al. 2017). The results suggest that antagonistic interactions between polyamines and ethylene respond to moderate soil-drying, and consequently,mediate spikelet development in rice.

It is proposed that salicylic acid (SA), another type of new plant hormone, may also be involved in regulating spikelet degeneration under abiotic stress. There is report showing that spraying SA to heat-stressed plants significantly increased concentrations of soluble sugars,proline, phytohormones including ABA, GA3, BRs, IAA, and ZR and activities of antioxidant enzymes in rice panicles,and reduced the spikelet degeneration rate (Zhang C X et al. 2017). However, the effect of applying SA on spikelet degeneration and grain yield was not detectable when plants were grown at normal growth conditions, suggesting that SA plays a role in alleviating spikelet degeneration only under heat stress.

It should be noteworthy that the structure of inflorescence of spikelet in rice is largely differed with that in wheat and maize (Smith 1995). In rice, spikelet is equal to floret since one spikelet consists of one floret. In wheat, one spikelet is consisted of 7–10 florets. Several distal florets of them are degenerated. In ear of maize, one spikelet is consisted of two florets. The difference in the structure of inflorescence among cereal crops may have different mechanisms in spikelet or floret degeneration.

3. Cultivation techniques for reducing the degeneration of spikelets in rice

Studies on the agronomic practices to regulate the differentiation and degeneration of rice spikelets are mainly concentrated on N application and water management(Matsushima 1980; Saini 1997; Ghaley 2012; Ferrante et al. 2013; Zhang et al. 2013; Wu et al. 2017; Zhang W Y et al. 2017). It is observed that application of N fertilizer at panicle initiation could increase spikelet differentiation,while applying N from pistil and stamen differentiation to meiosis could significantly reduce spikelet degeneration(Matsushima 1980; Ghaley 2012; Zhang et al. 2013).The growth stage of meiosis is generally believed to be very sensitive for rice to respond environment changes,and spikelet degeneration will be substantially increased subjected to drought or to high/low temperature during this period (Saini 1997; Saini and Westgate 2000; Yokoyama et al. 2002; Boyer and Westgate 2004; Yang et al. 2007a).Some studies have shown that spikelet abortion and barrenness also happen when rice plants encounter unfavorable conditions from the filling of pollen grains to the heading stage, and therefore, rice plants are usually well-watered from meiosis to flowering to protect spikelets from degeneration and sterility (Itoh et al. 2005; Li et al.2009; Tan et al. 2011; Wang et al. 2012; Zhang W Y et al.2017). There are reports showing, however, that moderate soil drying or adoption of the irrigation with alternate wetting and moderate drying, that is soil water potential is not lower than –15 kPa or midday leaf water potential is not lower than–1.2 MPa, could promote spikelet differentiation and suppress spikelet degeneration, leading to more number of spikelets on a rice panicle when compared with continuous flooding (Zhang et al. 2009; Liu et al. 2013,Wang et al. 2016; Zhang W Y et al. 2017; Zhang 2018).Other cultivation techniques, such as proper plant density,could also decrease spikelet degeneration by reducing the difference between the differentiated and degenerated spikelets per panicle (Matsushima 1980; Horie et al. 2005;Tang et al. 2017). The mechanism underlying the effect of N application, water management, and plant density on spikelet degeneration, however, is yet to be understood.

4. Concluding remarks

Spikelet degeneration is a serious physiological defect and a major constraint in the grain production of cereals (Li et al.2009; Tan et al. 2011; Wang 2011; Zhang W Y et al. 2017;Zhang 2018). Elucidating the mechanism underlying spikelet degeneration is a big difficult problem of science (Wang 2011). Although some investigations have been made on the causes of spikelet degeneration, the mechanism remains unclear. Phytohormones play important roles in regulating spikelet degeneration (Brenner and Cheikh 1995; Yang et al.2001; Davies 2004; Pandey 2017). However, knowledge on the cross-talk among/between hormones in enhancing or suppressing spikelet degeneration is very limited. Further investigations are needed to: (1) understand the cross-talk among/between phytohormones, especially the interaction among BRs, PAs, and ethylene on spikelet degeneration;(2) reveal the physiological and molecular mechanism in which phytohormones and their interactions regulate the degeneration of spikelets; and (3) exploit approaches to decrease spikelet degeneration and to elucidate their mechanism.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31471438 and 31771710), the National High-Tech R&D Program of China (863 Program,2014AA10A605), the National Key Research and Development Program of China (2016YFD0300206-4), the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD), and the Top Talent Supporting Program of Yangzhou University, China (2015-01).

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