1. Introduction
Lodging severely reduces the grain yield and quality of rice [
1]. Furthermore, it increases production costs by adversely affecting the harvest manipulations and heightening the grain drying demand [
2,
3]. According to a study by Nakajima et al. [
4], rice lodging could also aggravate mycotoxin pollution that threatens animal and human health. Since the initiation of the ‘‘Green revolution’’ in the 1960s, semi-dwarf cultivars of rice and wheat have been developed, which have enhanced the lodging resistance significantly and increased global grain production [
5,
6,
7]. However, with the large-scale cultivation of high-yielding cultivars, extensive use of fertilizers, and simplified planting techniques, such as direct-seeding, the potential risk of lodging has increased in recent years [
8,
9,
10]. Thus, lodging-resistant cultivars have been developed as a genetic improvement strategy to increase the yield of rice, wheat, and other crops [
11,
12,
13,
14].
Lodging, which results from a loss of balance in plant bodies, refers to the lasting vertical stem displacement of plants [
15]. In the case of rice, there are three types of lodging: culm bending, culm breaking and root lodging [
3,
16]. Culm breaking is generally seen at the lower internodes (including the third and fourth internodes from the plant top), which happens when the bending moment of the upper plant part is excessive [
2,
17]. The manner in which rice resists against culm breaking is usually assessed by the lodging index (LI) [
18,
19,
20,
21]. A decrease in the LI indicates a stronger lodging resistance capability. Several studies have investigated the correlation of LI with lodging-related traits [
22,
23,
24]. However, as the LI is a ratio of the bending moment of the whole plant (BM) to the bending moment at breaking (M), it is inadequate for evaluating the lodging resistance capability under certain special conditions. For example, when the multiple differences in BM values between two cultivars are similar to the multiple differences in M values between the two cultivars, the calculated LI values of the two cultivars would exhibit no significant difference, which could be contradictory to the actual lodging resistance of the rice cultivars. As a result, an optimized parameter △BM (equal to the value of 2M minus the value of BM), which was defined as the external force that the basal second internode could withstand, was proposed to be used along with the LI for a further accurate evaluation of the lodging resistance [
25]. An increase in the △BM indicates a stronger lodging resistance capability. Lodging generally happens at the stage of grain filling [
26,
27]. In the research of Ichii and Hada [
28], the stem-breaking strength decreased to the minimum value and the LI increased to the maximum at 30 days after heading, which indicated that the grain-filling stage is the period when lodging often occurs. Lodging is associated with several biotic and abiotic factors: the height and weight of the plant, the length of the panicle, the plumpness of the leaf sheath, as well as the length, diameter and thickness of basal internodes influence the lodging resistance of rice [
29,
30,
31,
32,
33,
34]. Regarding the morphological factors, the external diameter and thickness of the cross-section from basal internodes strongly influence the breaking strength of the stem [
21,
35]. Additionally, the stem contents of soluble sugars, K, Si, cellulose, starch and lignin affect the basal stem-breaking strength pronouncedly [
36,
37,
38,
39,
40]. However, some researchers have suggested that the basal stem-breaking strength is decided by structural carbohydrates (lignin and cellulose) rather than non-structural carbohydrates (soluble sugars and starch) [
20,
41]. Growth conditions, such as the application of different fertilizers, planting density, direct seeding methods, and sheath blight attacks, strongly affect the lodging resistance of rice plants [
10,
19,
42,
43,
44,
45]. Lodging is also correlated with varying environmental parameters, such as rain, wind, CO
2, deep water, and resource complementarities [
46,
47,
48,
49,
50].
With the increase in depletion of the stratospheric ozone, atmospheric levels of greenhouse gases, land-use alterations and aerosol outputs, an increase in global temperatures (global warming) and a decrease in solar radiation in Asia have been recorded in recent decades [
51,
52,
53,
54]. In the last century, the average global surface temperature recorded an elevation by 0.5 °C, and its estimated range of elevation is 0.3–6.4 °C by the end of this century [
55]. An average annual reduction of 0.51 ± 0.05 W m
−2 in solar radiation in Asia has been reported [
56,
57]. Many studies have shown a significant influence of the increase in global temperatures on the yield and quality of rice grains [
58,
59]. Additionally, the positive role and significance of solar radiation in rice grain output have also been shown [
60,
61]. However, few studies have considered the influences imposed on rice lodging resistance by the solar radiation and temperature variations. One study reported that an increase in the soil temperature increased the lodging risk of rice plants [
18]. The low solar radiation reduced the physical strength of the stem and, thus, increased lodging susceptibility in rice [
62].
More than half of the global population consumes rice as a staple food. Since lodging, high temperature, and low solar radiation have detrimental effects on rice production, understanding the effects of temperature and solar radiation on lodging is important for growing rice that is adapted to the changing global climate. In the present work, we chose two eco-sites to carry out 3-year field experimentations on three sowing dates per year, to grow rice at different temperatures and under different solar radiation treatments. A total of 32 rice cultivars with different lodging resistance capabilities were evaluated under different combinations of temperature and solar radiation. Among them, 12 indica rice cultivars, which did not lodge in all the sowing dates based on the field observation, were selected for analysis. The objectives of the present study were to: (1) investigate the responses of the lodging resistance of indica rice cultivars to different temperature and solar radiation treatments; (2) evaluate the most and least affected cultivars among the 12 indica rice cultivars under different temperature and solar radiation treatments; (3) explore the relationship of the morphological, mechanical, and biochemical characteristics associated with lodging resistance with temperature and solar radiation. To cope with global climate change, a greater understanding of the climatic impact on lodging in indica rice will provide guidelines for rice breeders to adopt appropriate strategies for developing lodging-resistant indica rice cultivars in the future.
4. Discussions
As both of the experimental sites have a subtropical monsoon type of climate, the temperatures gradually increase from spring to summer and decrease in autumn (
Figure 1). However, Xindu is in the basin area, while Ezhou is in the plain area. Xindu is situated at a higher altitude than Ezhou. The differences in topography and altitude generate different temperature and solar radiation conditions between the two locations (
Figure 2). Rice is often sown in the late spring at Xindu and Ezhou, and delayed sowing will make rice suffer from high temperatures sooner. Since high temperatures accelerated the growth of rice and advanced the rice maturity [
78,
79], the determined growth durations reduced with the delay in the sowing dates (
Table 1). Hence, the average daily temperatures (
Tmean) during the determined growth durations increased with the delayed sowing dates (
Figure 2). As a high temperature tended to be accompanied by higher solar radiation [
69], the average daily solar radiation (
Rmean) also increased with the
Tmean from SD7 to SD9. However, the
Rmean varied little from SD1 to SD3 and even decreased from SD4 to SD6. This was due to the increase in cloudy and rainy days, which resulted in low sunshine hours and solar radiation. Delayed sowing can enhance the lodging resistance in winter wheat [
80]. However, the lodging resistance of
indica rice cultivars weakened with the delayed sowing dates in our research (
Figure 3). Therefore, optimizing sowing dates could be a useful strategy for improving lodging resistance and growing crops to adapt to climate change.
In this study, we found that whether the range of the
Tmean was less than 1 °C across the three sowing dates in each year or more than 4 °C across the two locations (
Figure 2), the increased
Tmean significantly decreased the lodging resistance of
indica rice cultivars (
Figure 4A,E and
Figure 5A,E), which indicated that the lodging resistance was more sensitive to the
Tmean than the other temperature and solar radiation parameters. This could also be demonstrated by the results of stepwise regression analysis and path analysis. However, the response of the lodging resistance to other crops could be different. Previous research found that high temperatures showed an inconsistent effect on the stem-lodging resistance in canola plants, but reduced the root-lodging resistance significantly [
81]. The results of stepwise regression analysis and path analysis also showed that the
Rmean had a positive effect on the lodging resistance (
Figure 5,
Table 4). That is to say, an increase in the
Rmean would improve the lodging resistance. However, this effect was not detectable under the greater negative influence of increased
Tmean on the lodging resistance across the three sowing dates in 2018 and across the two locations (
Figure 4C,G and
Figure 5C,G). However, the lodging resistance displayed a slightly increasing trend from 2017 to 2018 at Ezhou (
Figure 5C,G). We inferred that the positive effect of the increased
Rmean on the lodging resistance outweighed the negative effect of the increased
Tmean because of the larger differences (△
Rmean = 2.1 MJ m
−2 d
−1) in the
Rmean than the differences (△
Tmean = 0.8 °C) in the
Tmean between 2017 and 2018 at Ezhou (
Figure 2). Several researchers found that low solar radiation could promote the vertical elongation of plants, such as an increase in the internode length and plant height, and restrain the lateral growth, such as a decrease in the culm diameter and wall thickness, and reduce cell wall carbohydrates; thus, low solar radiation could cause crop lodging [
82,
83,
84,
85,
86,
87]. Our results were similar to the previous findings, i.e., the
Rmean was positively correlated with the lodging resistance. However, under the conditions of our present study, since the
Tmean had a greater effect than the
Rmean (
Table 4), we could not establish the relationship between solar radiation and lodging-related traits.
According to the correlation analysis between the
Tmean and lodging-related traits (
Table 5), we found that with the increased
Tmean, it was mainly the reduction in breaking resistance (BR) and the bending moment at breaking (M) of the basal second internode that weakened the lodging resistance of
indica rice cultivars. The decreased stem-bending strength due to short periods of high temperature stress could also be found in canola [
88]. In addition, the stem length (SL) of the basal second internode increased significantly with the increased
Tmean, which could be a reason for the decline in the BR [
89].
The culm stiffness of rice plants, which is expressed by the bending stress (BS), is a product of the structural carbohydrates (primarily lignin and cellulose) and non-structural carbohydrates contents at the lower internode. Carbohydrates in rice culms are accumulated before heading and transported to the ears after heading and it is mainly the non-structural carbohydrates which are transported to grains for grain filling [
90,
91]. Thus, the culm stiffness increases with more structural carbohydrates in the basal stems [
33,
41]. Li et al. [
92] observed that the cellulose content (CC) of rice
brittle culm1 (
bc1) was lower than that of the wild type, but the lignin content (LC) was higher. However, the total content of lignin and cellulose (TC) of
bc1 was lower than that of the wild type, which led to the weaker culm strength of
bc1. In our study, the increase in LC was more than the decrease in CC as the
Tmean increased. As a result, the TC increased with the
Tmean, which caused the increased BS (
Table 6). The physical strength of the culm, which was represented by the M value, was significantly and positively correlated with the BS and section modulus (SM) [
20,
32]. Despite the BS increasing with the
Tmean, the decrease in the SM was even more important with the higher correlation coefficient, which was responsible for the significant reduction in the M value (
Table 6). Additionally, the decrease in the SM was attributed to the reduced culm diameter (CD) and culm wall thickness (CT) of the basal second internode with the increased
Tmean. As a consequence, CD, CT, and SL were the major factors influencing the physical strength of the culm under the effect of temperature.
The soil properties of the experimental fields at Xindu and Ezhou were different, which might affect the lodging resistance of tested rice cultivars. However, rice had been cultivated in the experimental fields for many years, which indicated that the soil properties were suitable for rice growth and development. In addition, the fertilizer applications between the experimental fields at Xindu and Ezhou were identical, resulting in a similar uptake of nitrogen, potassium and silicon from the soil, which caused the soil properties to have little influence on the lodging resistance [
93]. In the research of Niu, Feng, Ding and Li [
47], strong wind and heavy rain were the two most important causes of lodging. Even though there was no strong wind and heavy rain during the determined growth durations in our study, we selected 12
indica rice cultivars which did not lodge in the fields for analysis in order to exclude the influence of wind and rain on the plant lodging. Therefore, ordinary wind and rain had little effect on the lodging resistance of
indica rice cultivars.
Although the lodging resistance of 12
indica rice cultivars significantly weakened with the increased temperature, each of the cultivars responded differently to the temperature (
Table 3). The lodging resistance of lodging-moderate cultivar Chuanxiang 29B was most affected by the temperature with the highest coefficient of variation, and that of lodging-resistant cultivar Jiangan responded least to the temperature with the lowest coefficient of variation. This implied that the lodging-resistant
indica cultivar had the potential to adapt to a higher temperature.