Chen Yibo, Zhao Lei, Wang Chongrong, Li Hong, Huang Daoqiang, Wang Zhidong, Zhou Degui, Pan Yangyang, Gong Rong, Zhou Shaochuan

Letter

Stay-Green Panicle Branches Improve Processing Quality of Elite Rice Cultivars

Chen Yibo#, Zhao Lei#, Wang Chongrong, Li Hong, Huang Daoqiang, Wang Zhidong, Zhou Degui, Pan Yangyang, Gong Rong, Zhou Shaochuan

(Rice Research Institute, Guangdong Academy of Agricultural Sciences / Guangdong Key Laboratory of New Technology in Rice Breeding / Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou 510640, China; These authors contributed equally to this work)

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Rice panicle branches are key routes for transportation of photosynthetic products to grains. Branch senescence is an important trait that the breeders considered when breeding elite rice cultivars in South China. However, little is known about the mechanisms underlying the contributions of stay-green panicle branches to rice yield and quality. Here, we reported stay-green branches that continuously maintained transportation function and provided carbohydrates for basal grain development at the late stages of rice development. This ensured the coordination of development between apical and basal grains, and further improved the processing quality of elite rice. These findings provided strategies for improving the fullness and quality of rice grains and presented an important basis for cultivating elite rice.

Rice (L.), one of the most important crop species in the world, is the staple food for more than half of the global population (Zhai et al, 2018; Zeng et al, 2021). Improving rice yield and quality is the most important goal for breeders and scientists. Senescence, the final stage of development, is an active phase of orderly degradation and remobilization process, involving a series of changes at the cellular, tissue, organ, and organism levels, and thus it directly affects the yield and quality of crops (Gregersen et al, 2013; Gan, 2018; Chu et al, 2021). It is estimated that rice yield can be theoretically increased by 2% if the life of functional leaves was prolonged by 1 d at the maturity stage (Liu, 1983). Many studies have explored the molecular mechanism of senescence in rice. Thealleles introgressed into- type cultivars in Korean rice result in delayed senescence, with increased grain yield and enhanced photosynthesis (Shin et al, 2020). Xue et al (2021) revealed that an MYB transcription factor involved in the flavonoid pathway exhibits different anti-senescence leaf patterns among rice cultivars in South China. The senescence database also provides comprehensive information concerning senescence-associated genes and their corresponding mutants (Li et al, 2014).

Previous studies have mainly focused on the senescence of rice leaves, but the senescence of panicle branches, as a function of flow, has rarely been studied. Panicle branch is the key route for transportation of photosynthetic products from the source to the sink (Chang et al, 2020). During the maturity period, breeders tend to select stay-green panicle branches and stalks, which are bluish-green, functional and non-wilted, and are called ‘green branches and yellow wax stalks (Qingzhilagao)’ (Lin et al, 1987). These traits are typical for elite rice in Guangdong Province, China. Currently, breeders in Guangdong have developed many rice cultivars with the Qingzhilagao characteristics, which are widely grown in the rice regions of southern China, and are recognized for their high qualities and yields. However, there is scarce research on the contribution of anti-senescent panicle branches to yield and quality in elite rice cultivars.

Fig. 1.Stay-green panicle branches promote grain development and head rice rate at the maturity stage of rice development.

A, Morphologies of panicle branches and grains from MXZ and WSSM cultivars. Red arrow indicates panicle branches. B and C, Chlorophyll content (B) and head rice rate (C) of apical and basal panicles in eliterice cultivars at 30 d after flowering (DAF).D and E, Chlorophyll content (D) and soluble sugar content (E) of apical and basal panicle branches in MXZ and WSSM at 8, 18, 23, and 30 DAF. F and G, Soluble sugar (F) and starch content (G) of apical and basal grains in MXZ and WSSM at 8, 18, 23, and 30 DAF. MXZ, Meixiangzhan 2; WSSM, Wushansimiao.

Data are Mean ± SD (= 3).

In this study, cultivars were divided into two groups (stay-green and early-senescence), based on the differences in the chlorophyll content at 30 d after flowering (DAF). We used Meixiangzhan 2 (MXZ, one of the most favorablerice in China) and Wushansimiao (WSSM) as representatives (Fig. 1-A). We found that the apical branches of the stay-green cultivar (MXZ) remained green and alive, instead of wilting in early-senescence cultivar WSSM (Fig. 1-A). To explore the relationship between the senescence of branches and grain traits, the chlorophyll content and unfilled grain ratio were detected in 10 rice cultivars (Table 1). The average proportion of unfilled grains of stay-green rice cultivars was approximately 4%, whereas that of early-senescence rice cultivars was approximately 16% (Table 1). This indicated that the senescence traits of branches significantly affected grain development.

We further analyzed 11 rice grain traits including amylose content, grain length, and head rice rate of 16 rice cultivars (Table S1). A correlation analysis revealed that the chlorophyll content index significantly influenced the head rice rate, brown rice rate and milled rice rate, but had no significant influence on the other grain traits were found (Table S2). The differences in chlorophyll content and head rice rate between the apical and basal branches of stay-green type rice were small (Fig. 1-B and -C). In contrast, the differences in the early-senescent type rice were more significant between the apical branches and the basal branches (Fig. 1-B and -C, Table S1). The results showed that stay-green branches ofrice may be beneficial for rice processing quality. We speculated that stay-green branches ofrice may increase grain maturity, which, in turn, can lead to improved processing quality.

To explore how the senescence characteristics of branches affect grain development, the chlorophyll and soluble sugar contents of the apical and basal branches in MXZ and WSSM were detected at 8, 18, 23, and 30 DAF (Fig. 1-D and -E). The chlorophyll contents of both MXZ and WSSM decreased with grain development, indicating continuous senescence (Fig. 1-D). Nonetheless, compared with the early-senescent branches of WSSM, the change in the chlorophyll content of the stay-green branches of MXZ was less, and the difference between the apical and basal branches was also less, especially at 30 DAF (Fig. 1-D). Compared with WSSM, the chlorophyll contents of MXZ branches were higher at 18–30 DAF. The soluble sugar contents of the apical and basal branches of MXZ reached a peak at 18 DAF, which were earlier than the peak at 23 DAF in WSSM (Fig. 1-E). The soluble sugar contents of the apical and basal branches of MXZ were significantly higher than that of WSSM at 30 DAF. These results showed that the soluble sugar contents (the major photosynthetic product) of stay-green branches reached a peak faster than those of the early-senescent branches and can maintain a high concentration at 30 DAF, indicating that the stay-green branches may have strong transportation capacity.

Table 1. Chlorophyll content of panicle branches and unfilled grain ratio of stay-green and early-senescence elite indica rice cultivars.

The unfilled grain ratio was calculated as the ratio of the fresh weight of unfilled grains to the total fresh weight of unfilled and filled grains.Data are Mean ± SD (= 3). ** indicates significant difference at< 0.01.

We further assessed the changes in the soluble sugar and starch contents of the grains of MXZ and WSSM at 8, 18, 23, and 30 DAF (Fig. 1-F and -G). The soluble sugar content peaked at 8 DAF in the two cultivars. The soluble sugar contents of the apical and basal grains in MXZ were higher than those in WSSM at 8 DAF. Compared with WSSM, the soluble contents of MXZ branches were higher, and the difference between the apical and basal branches was smaller at 30 DAF. The difference in starch content between the apical and basal grains of MXZ was small, whereas that of WSSM was significant during the period from 8 to 30 DAF. These results indicated that the soluble sugar and starch content of grains between the two cultivars differed significantly as a result of the senescence characteristics of the branches.

In China, increasing grain yields is a primary concern for rice breeders. As a result, high-yielding cultivars with numerous spikelets on a panicle are cultivated. However, these cultivars often fail to achieve high-yield due to poor grain-filling of later-flowering inferior spikelets. Previous studies have showed that the average filling proportions of inferior spikelets were 20.7% in 12 ‘super’ rice cultivars, which are lower than those of superior spikelets in three conventional cultivars (6.3% on average) (Cheng et al, 2007; Yang and Zhang, 2010). These studies mainly focused on the development mechanisms of spikelets and their grains, and suggested that key enzymes (rather than carbohydrates) limit grain-filling in inferior spikelets (Yang and Zhang, 2010). In this study, we found that properly delaying senescence of the branches was beneficial to grain development and quality. Continuous material supply later at the grain maturity stage has been proved to promote the formation of orderly packed starch granules and protein bodies, which contributes to excellent rice grain qualities (An et al, 2020). We speculated that stay-green branches have strong anti-senescence ability, and may maintain continuous transportation function and continuously provide carbohydrates for basal grain development at the late stages of rice development. This ensured the coordination of grain development between the apical and basal parts and further improved the processing quality of rice.

It is widely accepted thatrice is less susceptible to senescence than(Abdelkhalik et al, 2005). In fact, according to our observations, the panicle branches of mostcultivars exhibited anti-senescence compared with, and their basal grains were usually fully matured, which is very rare in high-yieldingcultivars. Currently, the synergistic improvement of rice yield and quality has encountered a bottleneck (Huang et al, 2022). We believe that improving the vigor of panicle branches may be an effective strategy. We tried to use the strategy of-cross to introduce the stay-green branches ofrice intorice and have made good progress thus far.

In conclusion, stay-green branches continued to transport photosynthetic products to the grains at the late stages of rice development, which is beneficial for grain development and quality. Our results can inform new strategies for improving basal grain filling.

ACKNOWLEDGEMENTS

This study was supported by the Laboratory of Lingnan Modern Agriculture Project, China (Grant No. NT2021001), the National Natural Science Foundation of China (Grant No. 31801448), the Special Fund for Scientific Innovation Strategy- Construction of High Level Academy of Agriculture Science, China (Grant No. R2018PY-QF003), and the Special Fund for Science and Technology Innovation Strategy of Guangdong Academy of Agricultural Sciences: Dean’s Fund Key Project (Grant No. 202001).

SUPPLEMENTAL DATA

The following materials are available in the online version of this article at http://www.sciencedirect.com/journal/rice-science; http://ricescience.org.

File S1. Methods.

Table S1. Grain quality of cultivars with stay-green and early- senescent panicle branches.

Table S2. Correlation analysis of chlorophyll content with grain quality in cultivars.

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Zhou Shaochuan (xxs123@163.com)

17 May 2022;

31 August 2022

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Peer review under responsibility of China National Rice Research Institute

http://dx.doi.org/10.1016/j.rsci.2022.08.001