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The molecular mechanism of temperature regulation of rhizome development in perennial rice has been elucidated

author:Frontiers of Plant Science

Traditional agriculture mainly grows annual crops, which need to be cultivated repeatedly, which accelerates the consumption of land resources. While pursuing high yield and high quality crops, the application of a large number of chemical fertilizers, pesticides, herbicides, etc., eventually leads to environmental pollution, soil erosion, high carbon emissions, high consumption of natural resources, and large labor input (Crews et al. 2018). In addition, the natural stress resistance of these annual crops has gradually deteriorated after long-term artificial selection and meticulous field management, making it difficult for them to adapt to increasingly drastic environmental changes (Chapman et al. 2022). In the context of global climate change, people expect to establish a low-carbon emission, environmentally friendly, and sustainable agricultural production method.

Compared with annual crops, which require repeated cultivation, perennial crops have the advantage of no-tillage, which can be harvested for many years in a row, effectively reducing the risk of soil erosion (Glover et al. 2010). Moreover, perennial crops have large root systems, which can trap more carbon from the soil, increase soil fertility, and reduce carbon emissions from agricultural production activities (Peixoto et al. 2022). In addition, the cultivation of perennial crops can also reduce the input of labor, capital and natural resources required for agricultural production (Zhang et al. 2023), which has a positive effect on increasing farmers' income and maintaining food production in hollow villages.

The molecular mechanism of temperature regulation of rhizome development in perennial rice has been elucidated

Fig.1 Wild rice plants with long stamens

The white stalks are roots buried in the soil

Underground rhizomes are important organs for grasses to achieve perennial growth, and can survive harsh environments (such as low temperatures, droughts, etc.) in the soil. Among the rhizome type wild rice, only the wild rice with long stamen (referred to as Nagano) has the same AA genome as cultivated rice (Tao and Sripichitt 2000), and Nagano also has excellent agronomic traits such as resistance to diseases and pests (Sacks et al. 2003), which is an excellent germplasm resource for improving cultivated rice varieties and breeding perennial rice. Previous research found that the addition of sucrose could increase the number and length of rhizomes in Nagano (Fan et al. 2022). However, so far, the effects of other environmental factors on rhizome development in Nagano have not been reported.

Recently, the research group of Professor Yang Jiangyi of the State Key Laboratory of Conservation and Utilization of Subtropical Agricultural Biological Resources and the School of Life Science and Technology of Guangxi University published a research paper entitled "Temperature Effect on Rhizome Development in Perennial rice" in the SCI journal Rice, District 1, Chinese Academy of Sciences, which clarified the molecular mechanism of temperature regulation of axillary bud germination and rhizome upturning in Nagano. This study provides a new perspective for analyzing the relationship between temperature and rhizome development, which is helpful for the research and application of perennial rice.

Nagano has two types of lateral branches: tillers and rhizomes; Cultivated rice has only tillers. Unlike tillers, which grow upwards at the beginning, rhizomes grow laterally in the soil for a certain distance before they grow upside out of the soil and develop into aboveground stems (vegetative ramets) (Figure 1). The lateral growth distance of rhizomes (i.e., rhizome length) is greatly affected by the environment, and the length of rhizomes will be affected by seasonal differences, fertility differences, and soil moisture differences.

The molecular mechanism of temperature regulation of rhizome development in perennial rice has been elucidated

Fig.2 Effect of temperature on axillary bud germination in Nagano.

The white arrows in A refer to the germinating lateral branches (including tillers and rhizomes)

In this study, the effects of high temperature and low temperature on axillary bud development in Nagano were compared by various methods such as soil culture, hydroponics and tissue culture, and it was found that lower ambient temperature (17-19 °C) was more effective in promoting axillary bud germination in Nagano (Fig. 2A). At the same treatment time, the number of side branches in Nagano was significantly higher at low temperatures than in high temperature environments (28-30 °C) (Figure 2B).

The lower ambient temperature (17-19 °C) also enhanced the negative gravity of the lateral branches, resulting in rapid upturning of the rhizomes, resulting in a shorter rhizome length and a smaller angle to the mother stem (Figure 3). The difference in the expression of gravitational response genes IAA20, WOX6 and WOX11 (Zhang et al. 2018) between the upper and lower sides of rhizomes was used to analyze the effect of temperature on the gravity response of rhizomes. The qPCR results showed that the expressions of IAA20, WOX6 and WOX11 in the lower side of the rhizome were higher than those in the upper side. However, at lower ambient temperatures, the expression difference between IAA20 and WOX11 was greater than that at high temperature (indicating that the gravitational response was stronger at low temperature), while the expression difference between WOX6 and WOX11 was not affected by temperature.

The molecular mechanism of temperature regulation of rhizome development in perennial rice has been elucidated

Fig.3 Effect of ambient temperature on lateral branch angle and rhizome length in Nagano. The white arrows in A indicate the angle between the side branches of Nagano and the mother plant.

In order to explore the gene regulation pathways of low temperature promoting axillary bud germination and rhizome upturning, the differentially expressed genes in Nagano's basal shortened joints (with axillary buds) were analyzed by transcriptome sequencing and verified by qPCR. The results showed that plant hormones played an important role in temperature regulation of rhizome development in Nagano. The up-regulation of auxin distribution regulators ARF17, ARF25 and FucT (Wang et al. 2022) at low temperatures exacerbated the degree of auxin asymmetric distribution and induced enhanced asymmetric expression of WOX11 between the upper and lower sides of the rhizome, further leading to rapid upturn of the rhizome at low temperature (Fig. 4A). In the high temperature environment, the expression of auxin biosynthesis gene YUCCA1 and cytokinin oxidase/dehydrogenase genes CKX4 and CKX9 was up-regulated, and the expression of cytokinin synthesis gene IPT4 was down-regulated, which ultimately led to the decrease of cytokinin, which was not conducive to axillary bud germination. In addition, the D3 and D14 genes in the unicorn calolide signal transduction pathway, which negatively regulates axillary bud germination, were also up-regulated and inhibited axillary bud germination at high temperature. These results suggest that cytokinin, auxin, and unicornolide are jointly involved in the temperature-regulated germination process of axillary buds in Nagano (Fig. 4B).

The molecular mechanism of temperature regulation of rhizome development in perennial rice has been elucidated

Figure 4: Temperature regulation model of axillary bud germination and gravity response in Nagano.

Wang Kai, a doctoral student from the School of Life Science and Technology, Guangxi University, is the first author of the paper, and Associate Professor Yourong Fan and Professor Jiangyi Yang are the co-corresponding authors. The research was supported by the National Natural Science Foundation of China and the Guangxi Natural Science Foundation.

Original link: https://thericejournal.springeropen.com/articles/10.1186/s12284-024-00710-2

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The molecular mechanism of temperature regulation of rhizome development in perennial rice has been elucidated

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