Effects of increased ozone on rice panicle morphology

Guoyou Zhang; Yaxin Hu; Xiaoya Pan; Rong Cao; Qinan Hu; Rao Fu; Hamdulla Risalat; Bo Shang

doi:10.1016/j.isci.2023.106471

. 2023 Mar 23;26(4):106471. doi: 10.1016/j.isci.2023.106471

Effects of increased ozone on rice panicle morphology

Guoyou Zhang ^1,^5,^6,^∗, Yaxin Hu ^2,⁴, Xiaoya Pan ^3,⁴, Rong Cao ¹, Qinan Hu ¹, Rao Fu ¹, Hamdulla Risalat ¹, Bo Shang ¹

PMCID: PMC10122049 PMID: 37096034

Summary

Ground-level ozone threatens rice production, which provides staple food for more than half of the world’s population. Improving the adaptability of rice crops to ozone pollution is essential to ending global hunger. Rice panicles not only affect grain yield and grain quality but also the adaptability of plants to environmental changes, but the effects of ozone on rice panicles are not well understood. Through an open top chamber experiment, we investigated the effects of long-term and short-term ozone on the traits of rice panicles, finding that both long-term and short-term ozone significantly reduced the number of panicle branches and spikelets in rice, and especially the fertility of spikelets in hybrid cultivar. The reduction in spikelet quantity and fertility because of ozone exposure is caused by changes in secondary branches and attached spikelet. These results suggest the potential for effective adaptation to ozone by altering breeding targets and developing growth stage-specific agricultural techniques.

Subject areas: Pollution, Plant Biology, Plant morphology

Graphical abstract

Highlights

•
Short-term O₃ changes panicle traits in rice cultivars
•
Spikelets on secondary branches in rice panicles are very sensitive to O₃
•
Rice panicle responses to O₃ vary, depending on cultivars and growth stages
•
The results suggest more effective adaptations are needed

Pollution; Plant Biology; Plant morphology

Introduction

Rice (Oryza sativa L.), originally a wild grass, whose domestication could be traced back to over 10,000 years ago in the Yangtze Valley of China, is now the primary food source for more than half of the world’s population.¹^,²^,³^,⁴ Rice cultivation and production are not only the key to global food security but also shape the social economy and culture.⁵^,⁶ From a wild grass to a staple crop, the domestication of rice represents the transition of breeding from natural selection to artificial selection, and in the 1960s (the green revolution), the breeding of semi-dwarf rice varieties successfully increased yield potential.⁷^,⁸^,⁹

The ideal plant morphology in semi-dwarf varieties improves yield potential at the cost of high utilization of natural and agronomic resources,¹⁰^,¹¹^,¹² the wide cultivation of the high-yield varieties, in turn, accelerates climate change and environmental pollution.¹³^,¹⁴ Surface ozone (O₃), an air pollution, whose concentration is increasing¹⁵^,¹⁶^,¹⁷ because of climate change and environmental pollution, threatens rice production and food security.¹⁸^,¹⁹ Numerous studies have consistently demonstrated the negative effects of elevated concentrations of O₃ on rice.²⁰^,²¹^,²²

The effects of O₃ on rice have been studied from various aspects, including the physiological,²³^,²⁴^,²⁵ biochemical,²⁶^,²⁷^,²⁸ agronomical,²⁹^,³⁰ microclimatical,³¹ and ecosystematical³² impacts and the related mechanisms. However, the effects of O₃ on the morphological aspects of rice are not well clarified yet, especially for rice panicle, which is the key to rice yield.³³ The panicle traits determine not only the grain yield and grain quality in rice, but also the adaptability of the rice plant.³⁴^,³⁵^,³⁶ It is thus important to investigate the responses of panicle traits in rice to the pollution of surface O₃. A few studies addressing the negative effects of elevated concentrations of O₃ on rice yield revealed that, to some extent, the yield loss was induced by the reduction in spikelet number per panicle (SPP).³⁷^,³⁸^,³⁹^,⁴⁰ Moreover, variations exist among spikelets and their responses to abiotic factors depending on their panicle positions.⁴¹^,⁴²^,⁴³

These results suggest that the panicle morphology in rice could be affected by O₃, but direct study on the effects of O₃ on panicle traits is lacking, limiting the efficiency of breeding adaptable cultivars in the future.²⁴^,⁴⁴ Moreover, there are spatiotemporal variations in the O₃ pollution,⁴⁵^,⁴⁶ which means that future plants need to improve the adaptability to different kinds of O₃ pollution, for example, the long-term (covers the whole growing season) and short-term (happens at different growth stages) O₃ pollution.⁴⁷^,⁴⁸^,⁴⁹

To better understand the morphological response of rice panicles, so that more efficient adaptations like breeding tolerant cultivars could be conducted in the future, this open top chamber (OTC) experiment was used to investigate the changes in panicle traits in rice in response to long-term and short-term O₃ pollution. Our hypotheses are as follows: (1) The number of branches, particularly the primary branch per panicle, is mostly determined by genetic factors and will not be affected by O₃ treatments; and (2) spikelet quantity and fertility are likely to be affected by environmental factors and will be affected by O₃ treatments; and (3) the effects of short-term O₃ may be not as apparent as those induced by long-term O₃.

Results

Effects of ozone on the weight and length of panicle in rice cultivars

The panicle weight (PW) was reduced by the O₃ fumigation to an extent varied by the treatment and cultivar. In comparison with the PW in CF, the PW of SY63 was significantly reduced by TAJ-NF40, HAR-NF40, and NF40 by 13, 22, and 33%, respectively (Table 1). However, the PW of WYJ3 was not significantly changed (Figure 1A). Moreover, in comparison with the PW in NF40, the PW of SY63 was 46% and 55% larger in TAJ-CF and HAR-CF treatments, respectively. The effects of treatment, cultivar, and their interaction were also significant on the panicle length (PL). The mean value across the treatments, the PL of SY63 was 70% longer than that of WYJ3 (Table 1). PL of SY63 was 10% longer in HAR-CF than in NF40, and PL of WYJ3 was 10% shorter in TAJ-NF40 than in CF (Figure 1B). The ratio of PW to PL (PW/PL) was also significantly affected by the cultivar, treat and their interactions (Table 1), and mean across the treatments, PW/PL in SY63 was 33% larger than that in WYJ3. PW/PL in SY63 was 13% and 27% smaller in TAJ-NF40 and HAR-NF40 than in CF (Figure 1C), and in comparison with NF40, PW/PL was 49% larger in HAR-CF.

Table 1.

Panicle weight (PW), panicle length (PL), the ratio of PW to PL (PW/PL), number of primary branches per panicle (PBPP), number of spikelets per primary branch (SPPB), number of secondary branches per panicle (SBPP) and the number of spikelets per secondary branch (SPSB) in rice cultivars of SY63 and WYJ3 at different treatments

	PW		PL		PW/PL		PBPP		SBPP		SBPPB		SPPB		SPSB
Variable	p values
Cultivar	<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		0.0242		<0.0001
Treat	0.0005		0.0082		0.0078		0.0012		<0.0001		<0.0001		0.0044		0.2462
Cultivar x Treat	0.0009		0.003		0.0029		<0.0001		<0.0001		<0.0001		0.3513		<0.0001

Least square means by Cultivar

Cultivar	g panicle⁻¹		cm panicle⁻¹		g cm⁻¹		panicle⁻¹		panicle⁻¹		branch⁻¹		branch⁻¹		branch⁻¹
SY63	4.0		24.7		0.2		12.3		40.7		3.3		5.9		3.2
WYJ3	1.8		14.6		0.1		9.8		16.7		1.7		5.8		3.1

Changes vs CF (%)

	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3
TAJ-NF40	−13	6	3	−10	−13	−2	−8	−1	−13	−7	−6	0	−2	2	2	−7
HAR-NF40	−22	2	3	−7	−27	2	−11	4	−20	−6	−11	−5	−3	1	3	−8
NF40	−33	−1	−4	−8	−30	9	−9	9	−15	−2	−7	−6	−2	1	−2	2
TAJ-CF	−2	11	5	−2	−11	4	−3	6	1	−1	3	−1	3	3	1	1
HAR-CF	4	−3	5	−8	5	6	−1	1	9	−14	10	−7	1	3	3	−7

Changes vs NF40 (%)

	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3
TAJ-CF	46	12	9	6	27	−5	6	−2	19	1	11	5	5	2	3	−1
HAR-CF	55	−2	10	−1	49	−3	8	−7	29	−12	18	−1	3	2	5	−9

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TAJ-CF (Ozone was removed from the background air at the tillering and jointing stage), HAR-CF (Ozone was removed from the background air at the heading and ripening stage), NF 40 (Ozone pollution at a 40 ppb concentration plus the background ozone level), TAJ-NF40 (NF40 at the tillering and jointing stage), HAR-NF40 (NF40 at the heading and ripening stage).

O₃ changes the panicles in rice cultivars

Panicle weight (PW, A), panicle length (PL, B), the ratio of PW to PL (PW/PL, C), number of primary branches per panicle (PBPP, D), number of secondary branches per panicle (SBPP, E) and the number of secondary branches per primary branch (SBPPB, F) in a hybrid rice cultivar (SY63) and a japonica rice cultivar (WYJ3) at different treatments.

Effects of ozone on the number of primary and secondary branches in a rice panicle

The number of primary branches (PBPP) and secondary branches (SBPP) per panicle was significantly affected by the treatment, cultivar, and their interaction (Table 1). Both of the PBPP and SBPP in SY63 were more sensitive to the treatments than those in WYJ3 (Figures 1D and 1E). In comparison with the value in CF, PBPP of SY63 was significantly reduced by TAJ-NF40, HAR-NF40, and NF40 by 8, 11, and 9%, respectively (Table 1). The PBPP of SY63 in HAR-CF was 8% larger than that in NF40, and the difference was significant (Figure 1D). The SBPP of SY63 was 13, 20, and 15% smaller in TAJ-NF40, HAR-NF40, and NF40 than in CF (Table 1), and the difference was significant (Figure 1E). Compared with the value in NF40, SBPP of SY63 was significantly larger in TAJ-CF (19%) and HAR-CF (29%). The number of secondary branches per primary branch (SBPPB) was significantly affected by the treatment, cultivar, and their interaction (Table 1). SBPPB of SY63 was sensitive to the treatments. However, SBPPB of WYJ3 was constant, independent of the treatments (Figure 1F). In comparison with the value in CF, SBPPB of SY63 was significantly reduced by HAR-NF40 and NF40 by 11% and 7%, respectively. In comparison with the value in NF40, SBPPB of SY63 was significantly increased by HAR-CF by 18%.

Effects of ozone on the number of spikelets in a rice panicle

The number of spikelets per primary branch (SPPB) was significantly affected by the treatment and cultivar (Table 1). The SPPB of SY63 was 1.7% larger than that of WYJ3, and the mean across two cultivars, SPPB in TAJ-CF was 3.6% larger than that in NF40 (Figure 2A). The number of spikelets per secondary branch (SPSB) was significantly affected by the cultivar and the interaction of cultivar and treatment (Table 1). SPSB of SY63 was 3.2% higher than that of WYJ3, and SPSB of SY63 was higher in TAJ-NF40 and HAR-NF40 than in CF (Table 1), whereas SPSB of WYJ3 was lower in TAJ-NF40 and HAR-NF40 than in CF, but the differences were not statistically significant (Figure 2C). The number of spikelets on primary branches per panicle (SPB), the number of spikelets on secondary branches per panicle (SSB), and the number of spikelets per panicle (SPP) were significantly affected by the treatment, cultivar, and their interaction (Table 2). The SPB, SSB, and SPP of SY63 were 27, 156, and 87% larger than those of WYJ3, and were more sensitive to the ozone treatments (Figures 3A–3C). TAJ-NF40, HAR-NF40, and NF40 reduced SPB of SY63 by 9, 16, and 11%, respectively, when compared to CF values; SSB of SY63 was reduced by 12, 19, and 18%, respectively; and SPP of SY63 was reduced by 11, 18, and 15%, respectively, when compared to CF values (Table 2). Furthermore, when compared to NF40 values, SPB of SY63 in TAJ-CF and HAR-CF were 12% and 11% larger, respectively; SSB of SY63 in TAJ-CF and HAR-CF were 23% and 32% larger, respectively; and SPP of SY63 in TAJ-CF and HAR-CF were 18% and 23% larger, respectively.

O₃ alters the spikelets in rice panicles

Number of spikelets per primary branch (SPPB, A), number of fertile spikelets per primary branch (FSPPB, B), number of spikelets per secondary branch (SPSB, C) and number of fertile spikelets per secondary branch (FSPSB, D) in a hybrid rice cultivar (SY63) and a japonica rice cultivar (WYJ3) at different treatments.

Table 2.

Number of spikelets on primary branches (SPB), ratio of infertile spikelets on primary branches (RISPB), number of spikelets on secondary branches (SSB), ratio of infertile spikelets on secondary branches (RISSB), number of spikelets per panicle (SPP) and the ratio of infertile spikelets per panicle in rice cultivars of SY63 and WYJ3 at different treatments

	SPB		FSPB		RISPB		SSB		FSSB		RISSB		SPP		FSPP		RIS
Variable	p values
Cultivar	<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		0.0119		<0.0001		<0.0001		<0.0001
Treat	<0.0001		0.1276		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001
Cultivar x Treat	<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001

Least square means by Cultivar

Cultivar	panicle⁻¹		branch⁻¹		%		panicle⁻¹		panicle⁻¹		%		panicle⁻¹		panicle⁻¹		%
SY63	73		68		5		133		119		9		206		187		8
WYJ3	58		49		13		52		46		11		110		95		13

Changes vs CF (%)

	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3
TAJ-NF40	−9	−3	−10	13	74	−68	−12	−10	−10	−3	−18	−62	−11	−6	−11	4	30	−58
HAR-NF40	−16	2	−15	13	−3	−44	−19	−13	−17	−11	−9	−51	−18	−4	−18	3	20	−38
NF40	−11	5	−11	20	69	−56	−18	0	−30	8	327	−35	−15	4	−23	13	262	−45
TAJ-CF	0	4	1	5	45	0	2	−1	−4	4	106	−31	1	3	−3	4	133	−3
HAR-CF	−1	−3	−1	5	42	−40	9	−17	6	−21	129	9	5	−8	2	−8	106	−10

Changes vs NF40 (%)

	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3	SY63	WYJ3
TAJ-CF	12	0	13	−13	−14	129	23	−1	39	−3	−52	6	18	−1	27	−8	−36	76
HAR-CF	11	−7	12	−12	−16	37	32	−17	53	−27	−46	67	23	−12	32	−19	−43	62

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For the meaning of the abbreviations for the ozone treatments, please see the foot note of Table 1.

O₃ changes rice panicle branches

Number of spikelets on primary branches per panicle (SPB, A), number of spikelets on secondary branches per panicle (SSB, B), number of spikelets per panicle (SPP, C), number of fertile spikelets on primary branches per panicle (FSPB, D), number of fertile spikelets on secondary branches per panicle (FSSB, E), number of fertile spikelets per panicle (FSPP, F), ratio of infertile spikelet on primary branches in a panicle (RISPB, G), ratio of infertile spikelet on secondary branches in a panicle (RISSB, H) and ratio of infertile spikelets per panicle (RIS, I) in a hybrid rice cultivar (SY63) and a japonica rice cultivar (WYJ3) at different treatments.

Effects of ozone on the fertility of spikelets in a rice panicle

The number of fertile spikelets per panicle (FSPP) and the ratio of infertile spikelets per panicle (RIS) were significantly affected by the treatment, cultivar, and their interaction (Table 2). The FSPP of SY63 was 97% larger than that of WYJ3, and the RIS of SY63 was 37% smaller than that of WYJ3 (Table 2). The FSPP of SY63 in TAJ-NF40, HAR-NF40, and NF40 were 11, 18, and 23% lower than that in CF, and the differences were significant (Figure 3F). The FSSP of WYJ3 in HAR-CF was 19% lower than that in NF40. The RIS of SY63 in CF was 30, 20, and 262% lower than in TAJ-NF40, HAR-NF40, and NF40, respectively. The RIS of SY63 in NF40 was 36% and 43% lower than those in TAJ-CF and HAR-CF (Figure 3I).

The number of fertile spikelets on primary branches (FSPB) was significantly affected by cultivar and the interaction of cultivar with treat (Table 2). The FSPB of SY63 was 40% larger than that of WYJ3, and the RISPB of SY63 was 60% smaller than that of WYJ3 (Table 2). The FSPB of SY63 in TAJ-NF40, HAR-NF40, and NF40 were 10, 15, and 11% lower than that in CF, and the differences were significant (Figure 3D). The FSPB of WYJ3 in NF40 was 20% larger than that in CF. The ratio of infertile spikelets on primary branches per panicle (RISPB) was significantly affected by the treatment, cultivar, and their interaction (Table 2). RISPB of SY63 was constant in the treatments, whereas RISPB of WYJ3 was significantly affected by the treatments (Figure 3G), which in TAJ-NF40, HAR-NF40, and NF40 were 68%, 44%, and 56% lower than in CF.

The number of fertile spikelets on secondary branches (FSSB) was significantly affected by cultivar and the interaction of cultivar with treat (Table 2). The FSSB of SY63 in HAR-NF40 and NF40 was 17% and 30% lower, respectively, than in CF (Figure 3E). The FSSB of WYJ3 was constant, independent of the treatments. The ratio of infertile spikelets on secondary branches per panicle (RISSB) was significantly affected by the treatment, cultivar, and their interaction (Table 2). The RISSB of SY63 in NF40 was 327% higher than that in CF (Figure 3H), and the RISSB of WYJ3 in TAJ-NF40 and HAR-NF40 was 62% and 51% lower than that in CF, respectively.

Correlations and multivariate analysis

The multi-correlations of the SPP and other variables across the cultivars and treatments are shown in Figure S2. The top five variables that significantly correlated with SPP were SSB (0.99), FSSP (0.97), FSSB (0.96), SBPP (0.96), and SBPPB (0.89). The top five variables that significantly correlated with FSPP were FSSB (0.98), SPP (0.97), SSB (0.96), SBPP (0.93), and SBPPB (0.85). We then plotted the SPP and FSPP in SY63 and WYJ3 against SBPP, SBPPB, and SSB, respectively (Figure 4). The results of simple linear regressions between SPP and SBPP in SY63 and WYJ3 were significant (Figure 4A). The equations for SY63 and WYJ3 were: y = 3.85 X + 49.7 and y = 3.65 X + 48.5. The relations between SPP and SBPPB in SY63 and WYJ3 were also significant (Figure 4B), with the equations of SY63, y = 43.9 X + 61.3; and WYJ3, y = 21.1 X + 73.6. The relations between SPP and SSB in SY63 and WYJ3 were also significant (Figure 4C), with the equations of SY63, y = 1.17 X + 50.5; and WYJ3, y = 1.32 X + 40.8. The results of simple linear regressions between FSPP with SBPP, SBPPB, and SSB in SY63 and WYJ3 were significant (Figures 4D–4F), and the equations were as follows: SY63, y = 3.51 X + 44.1 and WYJ3, y = 2.72 + 49.6 for FSPP with SBPP; SY63, y = 38.1 X + 60.8 and WYJ3, y = 16.0 + 67.9 for FSPP with SBPPB; and SY63, y = 1.09 X + 41.2 and WYJ3, y = 1.01 + 42.5 for FSPP with SSB.

Correlations between spikelet number and the panicle traits

Number of spikelets per panicle (SPP) plotted against number of secondary branches per panicle (SBPP, A), number of secondary branches per primary branch (SBPPB, B) and number of spikelets on secondary branches in a panicle (SSB, C). And number of fertile spikelets per panicle (FSPP) plotted against SBPP (D), SBPPB (E) and SSB (F). p values and correlated r squares were estimated by simple linear regression.

Discussion

This OTC experiment was used to investigate the changes in panicle traits in rice in response to long-term and short-term O₃ pollution to better understand the morphological response of rice panicles, in order that more effective adaptations, such as breeding tolerant cultivars, could be conducted in the future. Our hypotheses were: (1) The number of branches, particularly the primary branch per panicle, is primarily determined by genetic factors will not be affected by O₃ treatments; (2) spikelet quantity and fertility are likely to be influenced by environmental factors will be affected by O₃ treatments; and (3) the effects of short-term O₃ may be less obvious because those induced by long-term O₃ have only been partially tested. In details, possible mechanisms and remaining uncertainties are discussed as follows.

Panicle weight and panicle length responses to ozone are rice cultivar and growth stage dependent

The PW of SY63 was more sensitive to O₃ than the PW of WYJ3 (Figure 1A). This is consistent with previous studies, which have revealed that hybrid cultivars have greater responses to O₃ than inbred ones.²⁸^,³⁷^,⁵⁰ The short-term and long-term O₃ reduced the PW of SY63 by 13% (TAJ-NF40), 22% (HAR-NF40) and 33% (NF40), respectively (Table 1). The reductions in PW of rice in response to long-term O₃ have been tested by other cultivars and studies.⁵¹^,⁵² Our results further revealed that both short-term and long-term O₃ reduce panicle weight in sensitive rice cultivars. The long-term O₃ studies revealed that O₃ reduces SPP and increases the ratio of infertile spikelets in rice,³⁹^,⁴⁰ and through the multivariate analysis, we found that besides PL and PW/PL, PW was significantly correlated with the number of spikelets and the ratio of fertile spikelets (Figure S2), suggesting the main reasons for the reduction in PW by O₃ are the suspensions on spikelet formation and grain filling.

The effect of short-term O₃ on PW at the heading and ripening stage (HAR-NF40, 22%) was more apparent than that at the tillering and jointing stage (TAJ-NF40, 13%), showing a significant difference between CF and HAR-NF40 (Figure 1A). These suggest that the responses of PW to O₃ are growth stage dependent, and that the heading and ripening stages are more sensitive. The growth stage dependent impacts on rice have been tested by other short-term abiotic stresses like high temperature and high nighttime temperature, revealing that the starch accumulation could be suspended,⁵³^,⁵⁴^,⁵⁵^,⁵⁶ and that the heading and ripening stages are more sensitive than other stages. Moreover, in comparison with the PW of SY63 in NF40, short-term O₃ removal at tillering and jointing (TAJ-CF) and at heading and ripening (HAR-CF) significantly increased the PW of SY63 by 46% and 55% (Table 1), and owing to the increments, the PWs of SY63 at CF, TAJ-CF, and HAR-CF were not significantly different (Figure 1A). These suggest that short-term O₃ removal could reverse the reductions in PW induced by long-term O₃. Changes in source supply may be related to PW delivery mechanisms.

PL was more tolerant to O₃ than PW in both SY63 and WYJ3, and the responses of PL to O₃ were cultivar dependent. Long-term O₃ had no effect on the PLs of SY63 or WYJ3, whereas short-term O₃ at the tillering and jointing stage (TAJ-NF40) reduced the PL of WYJ3 by 10% (Figure 1B), and short-term O₃ removal at the heading and ripening stage (HAR-CF) increased the PL of SY63 by 10%. These suggest that the responses of PL to O₃ are rice cultivar and growth stage dependent. The response of PL to O₃ has been found to be regulated by the ABERRANT PANICLE ORGANIZATION 1 (APO1) gene,⁵⁷ whose transcript level was oppositely regulated in different rice cultivars. APO1 also regulates cell proliferation in the meristem to control the changeover of meristem phases,⁵⁸ which upregulation and downregulation may thus be related to the increase and decrease of PL. PL may also potentially be impacted by cytokinin oxidase, an enzyme that breaks down the phytohormone cytokinin.⁵⁹ There is a need to conduct more research to determine how and why O₃impacts PL.

Ozone decreases the number of branches per panicle in sensitive rice cultivars

The responses of the PBPP, SBPP, and SBPPB to O₃ were also rice cultivar and growth stage dependent. The number of branches in SY63 was more sensitive to O₃ than that in WYJ3. The long-term and short-term O₃ significantly affected the PBPP (Figure 1D), SBPP (Figure 1E), and SBPPB (Figure 1F) in SY63, indicating that the suspension on branch numbers per panicle could be induced by both the long-term⁵⁷ and short-term O₃. On the basis of the results of this study, the negative effect of O₃ on PBPP, SBPP, and SBPPB (Figure S3) could also be reversed by short-term O₃ removal. Changes of SBPP (Figure E) to O₃ were more apparent than PBPP (Figure D), showing that the number of secondary branches is primarily responsible for the panicle structure’s response to ozone. Both of the primary and secondary branches in the rice panicle were reported to be regulated by DENSE AND ERECT PANICLE 2 (DEP2),⁶⁰ whose expression may be affected by O₃ and remains to be revealed in future studies.

Ozone-induced declines in spikelets per panicle are a result of fewer spikelets on secondary branches

In comparison to WYJ3, SY63’s SPB, SSB, and SPP were larger and more sensitive to ozone treatments (Figures 3A–3C). Both short-term and long-term O₃ significantly reduced the SPB, SSB, and SPP in SY63 (Table 2). The suspensions on spikelet formation in rice by long-term O₃ have been reported in several studies.²⁸^,³⁸^,³⁹^,⁵⁷ SY63’s panicles showed a significant reduction in size under long-term O₃,³⁸ which was because of both the inhibition of spikelet differentiation and the promotion of spikelet degeneration, which were both linked to a reduction in nitrogen and biomass accumulation up to the heading stage. Our results further revealed that: (1) both short-term and long-term O₃ reduce the number of spikelets per panicle in sensitive rice cultivars; (2) O₃-induced declines in spikelets per panicle are a result of fewer spikelets on secondary branches (Figure 4); and (3) the reductions in the number of spikelets per panicle in rice could be reversed by O₃ removal.

It is reported that exposure to long-term O₃ affected the level of the APO1 transcript in the other direction, rising in Sasanishiki (japonica) and falling in Habataki (indica), showing differences in the APO1 amino acid sequences between rice cultivars.⁵⁷ Expression of O₃ stress responsive genes may be the mechanism for the changes in the number of spikelets per panicle in rice and remains to be studied in the future.⁶¹^,⁶²^,⁶³ Besides, the regulation of spikelet degeneration in cereals is also mediated by phytohormones such as auxins, cytokinins, gibberellins, abscisic acid, and ethylene.⁶⁴ In rice, jasmonic acid controls the development of the spikelet,⁶⁵^,⁶⁶^,⁶⁷ whereas levels of some phytohormones (including jasmonic acid, abscisic acid, and jasmonoyl-L-isoleucine) that are known to help reduce O₃-induced leaf damage tended to be differentially regulated in different rice cultivars.⁵⁷ Thus, the differentially regulated levels of phytohormones and expressed genes may be the mechanism why O₃ reduces the number of spikelets per panicle, and O₃ removal could reverse the reduction. This remains to be studied in the future.

Spikelets on secondary branches are principally responsible for ozone-induced changes in rice spikelet fertility

Reduced spikelet quantity and spikelet fertility are some of the ways that ozone lowers rice yields.²⁴ The quantity of harvested spikelets is determined by SPP and the number of panicles. Reductions in the spikelet number and fertility in rice by long-term O₃ were tested by other experiments,³⁰^,³⁷^,³⁹ whereas it was normally measured by the ratio of infertile spikelets to all of the harvested spikelets. On the scale of a rice panicle, the SPP is determined by SSB and SPB, especially in SY63, whose SSB is much larger than SPB. Thus, changes in the traits (for example, the number, fertility, and grain weight) in SSB primarily determine the changes in the traits in SPP. The fertility of inferior spikelets was found to be more sensitive to long-term O₃ than that of superior spikelets,³⁹ in which the inferior and superior spikelets are similar to the SSB and SPB. Moreover, the number of fertile spikelets is mostly correlated with the number of fertile spikelets on secondary branches (FSPP versus FSSB in Figure S2) and the number of spikelets on secondary branches (FSPP versus SSB in Figure 4F), showing that the spikelets on secondary branches are mostly responsible for ozone-induced changes in rice spikelet fertility.

In SY63, both long-term and short-term O₃ reduced spikelet fertility (as shown by decreased FSPP and increased RIS in Figure 3), and the changes were more apparent in SSB than in SPB, and the effects on spikelet fertility were reversed by O₃ removal. For WYJ3, however, RIS was decreased by short-term and long-term O₃, and the effects were reversed by O₃ removal too. Variations in the response of rice cultivars to long-term O₃ show that the impacts of O₃ may be opposite depending on rice cultivars.³⁰^,⁵⁷^,⁶⁸ The increase and decrease in spikelet fertility caused by O₃ addition and removal may be related to dry matter partitioning⁶⁹ and remobilization,⁷⁰ the antioxidant defense system,⁷¹ and nitrogen utilization.²⁹^,⁷²^,⁷³

Conclusion

The impact of both short-term and long-term O₃ pollution on rice cultivars’ panicle structures was investigated using an open-top chamber experiment. Long-term and short-term O₃ pollution both change the structure of the panicle, especially in a hybrid cultivar. The quantity and fertility of spikelets on secondary branches as well as the number of secondary branches are principally responsible for ozone-induced changes in rice panicle. The mechanism underlying the panicle change in rice under ozone pollution may be related to genetic and physiologic regulations that remain to be studied in the future. Furthermore, the removal of O₃ at particular growth stages could reverse the effects of O₃ on panicle structure, raising the prospect of the emergence of agronomic adaptations that are dependent on growth stage.

Limitations of the study

Two rice cultivars were adopted in this study, whereas there are numerous varieties of rice, investigating more cultivars may provide more confirmed results and inspirable information, however, as there are size limitations from OTC system, FACE (free-air carbon dioxide enrichment)²⁰^,⁷⁸ are preferred to conduct future cultivar screening studies. The FACE system facilitates interactions between climatic and agricultural factors.⁷⁸ Future studies on the interaction between growth-stage-specific fertilization and ozone are highly recommended, as fertilizer level affects the amount and fertility of rice spikelet.⁷⁹^,⁸⁰ This study only analyzed the mature samples collected at the harvesting season, whereas it is important to understand panicle development for effective agricultural management.⁸¹ Developing effective management adaptations requires a better understanding of the integrated regulation of panicle development by genetic (breed), environmental (e.g., ozone), and agricultural (e.g., fertilizer) factors.

STAR★Methods

Key resources table

REAGENT or RESOURCE	SOURCE	IDENTIFIER
Biological samples

Panicles of hybrid rice cultivar SY63, treated by ozone pollutions	This paper; Reference introduction	https://doi.org/10.1186/s12284-018-0210-9
Panicles of japonica rice cultivar WYJ3, treated by ozone pollutions	This paper; Reference introduction	https://doi.org/10.1016/j.rsci.2016.02.002

Other

Field experiment facilities, samplings, raw and analyzed data	This paper; Reference	https://doi.org/10.1002/ael2.20093

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Resource availability

Lead contact

Further information and requests for resources should be directed to and will be fulfilled by the lead contact, Guoyou Zhang (zhang-guoyou@hotmail.com)

Materials availability

This study did not generate new unique reagents.

Method details

Experimental facilities and rice varieties

Jiangdu county, Yangzhou city, Jiangsu province, China (119°43′E, 32°25′N) is the location of the experimental site. Based on historical data (2009–2018), the mean temperature and precipitation at the experimental site were 16 °C and 1131 mm, respectively.⁷⁴ The open-top chamber (OTC) method was adopted in this study,⁷⁵ OTC (regular octagon with a side length of 2m, bottom area of 10 m² and a height of 2.3 m) replications for O₃ removal and O₃ pollution are three, respectively. Two rice varieties which are commonly planted in this area were adopted in this study: hybrid rice variety Shanyou 63 (SY63) and japonica rice variety Wuyujing 3 (WYJ3). SY63, which is a semi-dwarf hybrid variety, is the most widely planted hybrid rice in China.⁷⁶ WYJ3, which ranks among the top ten conventional varieties in terms of nationwide application acreage in China, has been the primary japonica rice variety commercially applied in Jiangsu province for the longest time.⁷⁷

Crop cultivation and ozone treatment

On May 20, 2020, seeds of SY63 and WYJ3 were sown on a nursery bed to grow seedlings. In compliance with the local agronomic measures, the seedlings of each cultivar were manually transplanted into pots (with a diameter of 22 cm and a height of 31 cm, filled with local farm land soil). The number of randomly transferred pots of plants to each OTC was 20 pots of SY63 and 20 pots of WYJ3, respectively. The concentration of O₃ in the OTCs that were used as O₃ pollution was 40 ppb plus the concentration of O₃ in the background air (NF40), and O₃ was removed by charcoal filter in the other OTCs (CF). Details about the OTCs and ozone generator (HY003, Chuangcheng Co., Jinan, China) could be found in our previous study.⁷⁴ Starting on July 25, 2020, and lasting until harvest, O₃ fumigation was applied during the day. The fumigation was not applied on rainy days.

Except for the long-term effects of CF and NF40, in which the plants’ growth from transplanting to maturity was either under CF or NF40 conditions. Bidirectional transfer of 5 pots in CF and NF40 OTCs was used to design the short-term effects of CF and NF40. The bidirectional transfer of pots was conducted on August 25 and September 18, 2020, respectively. Thus, besides CF and NF40, there were four treatments: fumigation of NF40 at the tillering and jointing (TAJ) stage (TAJ-NF40); fumigation of NF40 at the heading and ripening (HAR) stage (HAR-NF40); O₃ removal at the TAJ stage (TAJ-CF); and O₃ removal at the HAR stage (HAR-CF).

Sample collection and analysis

Physico-chemical maturity was determined when grain moisture content fell to 20% and 85% of the grains became straw-colored. At maturity, the plants were collected from the pots in each OTC. Ten panicles from each pot were collected, and in each panicle (Figure S1), the following information was inspected: panicle weight (PW), panicle length (PL), number of spikelets per panicle (SPP), number of fertile spikelets per panicle (FSPP), number of primary branches per panicle (PBPP), number of secondary branches per panicle (SBPP), number of spikelets per primary branch (SPPB), number of fertile spikelets on primary branches (FSPB), the ratio of PW to PL (PW/PL), the ratio of SB to PB (number of secondary branches per primary branch, SBPPB), infertile spikelets to total spikelets on primary branches (RISPB), infertile spikelets to total spikelets on secondary branches (RISSB), and infertile spikelets to total spikelets per panicle (RIS) were calculated for further analysis.

Statistical analysis was performed by the JMP software (SAS Institute, Cary, NC, USA). The individual OTC was used as the statistical unit (n = 3 OTCs). The averaged data from three to four pots per treatment were averaged for all response variables, and the averaged data were subjected to ANOVA by fitting the mixed-linear model to test the effects of treatment, rice cultivar, and their interaction. The Tukey’s Honestly Significant Difference (HSD) test was applied to identify significant posthoc differences.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (42077209, 30099413), the Open Project of Jiangsu Key Laboratory of Crop Genetics and Physiology (YCSL202004), and the Open Fund of Key Laboratory of Agrometeorology of Jiangsu Province (JKLAM2001). We also express our appreciation to Prof. Zhaozhong Feng, Prof. Qi Wang, Dr. Yansen Xu and Mr. Fangzhen Yang for providing assistance in the field and laboratory work.

Author contributions

G.Z.: Conceptualization; Formal analysis; Funding acquisition; Methodology; Software; Visualization; Project administration; Supervision; Writing – original draft; Writing – review and editing. Y.H.: Conceptualization; Investigation; Data curation; Software; Visualization; Writing – original draft; Writing – review and editing. X.P.: Investigation; Software; Visualization; Methodology. R.C.: Investigation; Methodology; Software. Q.H.: Investigation; Methodology; Software. R.F.: Investigation; Methodology. H.R.: Investigation; Methodology. B.S.: Investigation; Methodology.

Declaration of interests

The authors declare no conflict of interest.

Published: March 23, 2023

Footnotes

Supplemental information can be found online at https://doi.org/10.1016/j.isci.2023.106471.

Supplemental information

Document S1. Figures S1–S3

mmc1.pdf^{(2.1MB, pdf)}

Data and code availability

•
All data reported in this paper will be shared by the lead contact upon request.
•
This paper does not report original code.
•
Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Document S1. Figures S1–S3

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Data Availability Statement

•
All data reported in this paper will be shared by the lead contact upon request.
•
This paper does not report original code.
•
Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request.

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PERMALINK

Effects of increased ozone on rice panicle morphology

Guoyou Zhang

Yaxin Hu

Xiaoya Pan

Rong Cao

Qinan Hu

Rao Fu

Hamdulla Risalat

Bo Shang

Summary

Graphical abstract

Highlights

Introduction

Results

Effects of ozone on the weight and length of panicle in rice cultivars

Table 1.

Figure 1.

Effects of ozone on the number of primary and secondary branches in a rice panicle

Effects of ozone on the number of spikelets in a rice panicle

Figure 2.

Table 2.

Figure 3.

Effects of ozone on the fertility of spikelets in a rice panicle

Correlations and multivariate analysis

Figure 4.

Discussion

Panicle weight and panicle length responses to ozone are rice cultivar and growth stage dependent

Ozone decreases the number of branches per panicle in sensitive rice cultivars

Ozone-induced declines in spikelets per panicle are a result of fewer spikelets on secondary branches

Spikelets on secondary branches are principally responsible for ozone-induced changes in rice spikelet fertility

Conclusion

Limitations of the study

STAR★Methods

Key resources table

Resource availability

Lead contact

Materials availability

Method details

Experimental facilities and rice varieties

Crop cultivation and ozone treatment

Sample collection and analysis

Acknowledgments

Author contributions

Declaration of interests

Footnotes

Supplemental information

Data and code availability

References

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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