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Research Article Received: 14 March 2016

Revised: 20 July 2016

Accepted article published: 28 October 2016

Published online in Wiley Online Library: 5 January 2017

(wileyonlinelibrary.com) DOI 10.1002/ps.4471

Enhanced photosynthesis endows seedling growth vigour contributing to the competitive dominance of weedy rice over cultivated rice Lei Dai,a,b† Xiaoling Song,a† Baoye He,a Bernal E Valverdea,c and Sheng Qianga* Abstract BACKGROUND: Weedy rice, as one of the worst paddy field weeds worldwide, bears vigorous seedlings and dominantly competes with cultivated rice causing serious crop yield losses. To elucidate the causes of its stronger seedling vigour endowing its dominant competition with cultivated rice, comparative studies on seedling growth characteristics were conducted among six weedy rice biotypes and the two indica and japonica cultivars Shanyou-63 (SY-63) and Zhendao-8 (ZD-8), respectively, in the greenhouse. RESULTS: Weedy rice emerged 2 to 3 days earlier, rapidly grew 1.3–1.7 cm taller daily, produced more secondary adventitious roots and greater aboveground fresh biomass than cultivated rice. Moreover, weedy rice exhibited greater photosynthetic pigment content, net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, transpiration rate, and chlorophyll fluorescence kinetic parameters. An enhanced overall photosynthetic activity in weedy rices was attributed to the combined action of a larger antenna, more active reaction centres and higher quantum yield for electron transfer beyond QA . CONCLUSIONS: Enhanced photosynthesis of weedy rice at the seedling stage should be the main factor for leading to strong competitive dominance over cultivated rice. © 2016 Society of Chemical Industry Keywords: weedy rice; seedling growth characteristics; photosynthesis; competition

1

INTRODUCTION

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Weedy rice (Oryza sativa L.), also known as red rice (AA genome, 2n = 24), is one of the most persistent and noxious weeds widely distributed in rice fields.1 – 3 It belongs to the same biological taxon as cultivated rice (O. sativa L.) and occurs in most rice-growing regions worldwide. Weedy rice is similar to cultivated rice in morphology, physiology and biochemistry, but usually exhibits many weedy traits such as enhanced stress tolerance4,5 and competitive ability,6 – 8 seed shattering9 – 13 and dormancy14 – 16 that facilitate seed dispersal and persistence in the field, and seed longevity.17,18 These traits and con-specificity with cultivated rice make controlling weedy rice very difficult compared to other weeds. Weedy rice has infested and occurs widely in rice fields in south-east Asia, North America, south Europe, and Latin America.19 – 22 It has become one of three worst weeds together with species of Echinochloa and Leptochloa in paddy fields worldwide.23,24 Weedy rice can reduce the rice crop yield by 20% to 90% and even cause total crop failure depending on infestation levels, relative proportion to crop plants, duration of crop interference, and the type of rice cultivar or biotype of weedy rice involved.25 – 32 Its success as a competitor can be attributed to weedy rice being often taller than the crop and producing more tillers,33 – 36 tolerance to stress including deep sowing,4,37 cold stress38 and drought,5 and having greater N-use efficiency than cultivated rice.39,40 Pest Manag Sci 2017; 73: 1410–1420

Additionally, weedy rice germinates and emerges earlier and exhibits rapid seedling growth with a better developed root system than cultivated rice. These characteristics of weedy rice also contribute to its competitive advantage over cultivated rice. Delouche et al.24 summarised research results from 1978 to 1992, finding that non-dormant seeds of weedy rice germinated earlier than those of cultivars, and that they also developed the mesocotyl, coleoptile and plumule faster, being also superior to varieties for root length and dry biomass at the seedling stage. Weedy rice grows taller much faster than cultivated rice,34,35 but the mechanism bestowing strong vigour to weedy rice seedlings with earlier emergence and faster growth has not been properly addressed.



Correspondence to: S Qiang, Weed Research Laboratory, Nanjing Agricultural University, Nanjing 210095 Jiangsu, P.R. China. E-mail: [email protected]

† Lei Dai and Xiaoling Song contributed equally to this study a Weed Research Laboratory, Nanjing Agricultural University, Nanjing 210095, Jiangsu, P.R. China b College of Life Science and Technology, Henan Institute Science and Technology, Xinxiang 453003, Henan, P.R. China c Investigación y Desarrollo en Agricultura Tropical, S.A., Tambor, Alajuela 4050, Costa Rica

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Enhanced photosynthesis endows seedling growth vigour Seed size has been shown to affect seedling vigour in many species.41 – 45 Generally, large-seeded species perform better under a diversity of adverse establishment conditions.46 – 48 In the case of rice, Cui et al.49 identified that four quantitative trait loci (QTLs) for seed size and four QTLs for seedling characteristics shared several similar regions, suggesting a close relationship between seedling characteristics and seed size. However, the fact that even weedy rice biotypes having smaller seeds than the crop develop into more vigorous seedlings compared to cultivated rice indicates that other factors confer strong seedling vigour and competitive superiority to the weedy form. Photosynthesis, by which green plants transform light energy into chemical energy, is the plant basic physiological processes determining plant growth and development.50,51 Concenço et al.52 evaluated characteristics related to photosynthetic ability in hybrid and inbred rice cultivars, to determine their possible association with competitive ability. At the same competition levels or sowing densities, plants of the hybrid cultivar are more competitive than inbred plants; hybrid plants were superior as to the photosynthesis rate when competing with up to three non-hybrid plants. Jiang et al.53 suggested that an increase in grain yield of wheat was associated with the elevation of leaf photosynthetic rate. We hypothesise that differences in photosynthesis are responsible for the differential growth characteristics between weedy and cultivated rice seedlings. However, previous research has not addressed the contribution of photosynthesis to competitiveness of weedy rice. In the present study, we compared distinct indica and japonica weedy rice biotypes contrasting in genetic diversity and collected from the different latitudes with cultivated rice by growing them in a common garden. We assessed seed grain characteristics, emergence time, growth traits, photosynthetic parameters, photosynthetic pigment content, and chlorophyll fluorescence kinetic parameters aiming to elucidate the mechanism of enhanced competitive ability of weedy over cultivated rice.

2

MATERIALS AND METHODS

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2.2 Experimental methods 2.2.1 Seed characteristics Seed size (length, width and thickness), shape (ratio between length and width), weight, and hull and pericarp colours were determined as described by Chang and Bardenas56 and the standard evaluation system for rice available from International Rice Research Institute (IRRI).57 2.2.2 Experimental design Definite greenhouse experiments based of preliminary studies were conducted at Pailou Experimental Farm (118∘ 37′ E, 32∘ 02′ N), Nanjing Agricultural University, China, in 2011. Experimental pots were exposed to natural light and photoperiod (approximately 14/10 h day/night), and temperature fluctuating approximately 25–34 ∘ C during the growing period. Eight seeds each of the six weedy rice biotypes and the two cultivars were sown individually at 0.5 cm depth in five pots (30 cm diameter, 25 cm height, with hole in the bottom) previously filled with a clay loam of medium fertility (organic matter 2.8%, N 97 mg kg−1 , available P 52 mg kg−1 , available K 161 mg kg−1 ) and pH 7.1 from a rice experimental field. Four pots planted with each rice material were randomly selected for the experiment and emerged plants were thinned to four uniform and robust individuals at 9 days after sowing. Each pot was considered an experimental unit. Plants were irrigated by capillarity by placing pots in trays filled with water. 2.2.2.1 Seedling emergence. From 3 days after sowing, the number of the emerged seedlings (the tip of the coleoptile appeared above the soil surface) was recorded daily until no additional emergence occurred. Then emergence onset and continuing emergence was calculated. 2.2.2.2 Plant height, morphological characteristics and biomass production. Plant height of the four individuals in each pot was measured at 12, 18 and 24 days after sowing (DAS). The rest of the measurements were taken at 24 DAS. These included the morphological parameters, leaf length, width and area, leaf angle, maximum of root length, number of secondary adventitious roots, and above-ground fresh biomass, all measured according to the methods described by Chang and Bardenas56 and Dong et al.,58 as detailed in Table 1. 2.2.2.3 Physiological measurements. Physiological measurements included photosynthetic pigment (chlorophyll a, chlorophyll b, total chlorophyll, carotenoids) content, photosynthetic parameters (net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, transpiration rate), and chlorophyll fluorescence kinetic parameters. All of these physiological measurements were obtained from the top second leaf of uniform cultivated and weedy rice seedlings. Each single seedling of each pot was measured. 2.2.3 Photosynthetic pigment content Leaf photosynthetic pigments were extracted with a mortar and pestle in cold 80% acetone and a minute amount of quartz sand. The extract was centrifuged at 4 ∘ C for 5 min at 1 × g. Chlorophyll a (Chla), chlorophyll b (Chlb) and carotenoid (Car) contents were determined spectrophotometrically (Spectrascan UV 2600, Toshniwal Instruments Pvt. Ltd., Chennai, India) according to Kiran et al.,59

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2.1 Plant materials Six representative weedy rice biotypes, whose competitive abilities with the crop have been already characterised,8 were selected as experimental material based on our previous studies on genetic diversity and morphological characteristics of various weedy rice accessions from the north-east, eastern and southern areas of China.8,54 Accessions were collected in 2006 in the cities of Shenyang (WRLN003, 123∘ 21′ E, 41∘ 02′ N) and Dandong (WRLN004, 124∘ 17′ E, 39∘ 58′ N) in Liaoning province, Dongfang (WRHA010, 108∘ 40′ E, 19∘ 06′ N) in Hainan province, Maoming (WRGD008, 110∘ 50′ E, 21∘ 40′ N) in Guangdong province and Yangzhou (WRJS023, 119∘ 20′ E, 32∘ 20′ N) and Taizhou (WRJS013, 119∘ 57′ E, 32∘ 26′ N) in Jiangsu province. Indica cultivar Shanyou-63 (SY-63) and japonica cultivar Zhendao-8 (ZD-8), both widely cultivated in Nanjing city of Jiangsu province, were used as controls in the study. WRLN003 and WRLN004 belong to the sub-species japonica; the other four biotypes are indica. The genetic diversity, Shannon indexes of WRLN003, WRLN004, WRHA010, WRGD008, WRJS023 and WRJS013 were 0.009, 0.043, 0.318, 0.207, 0.201 and 0.117, respectively.54,55 Plants of each of the six weedy rice accessions were grown in the field under homogeneous conditions. Seeds were dried in nylon fabric packets and stored −20 ∘ C until used in the experiment. Seeds of all six weedy rice biotypes and two cultivated rice cultivars had at least 90% germination.

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Table 1. Measurement methods used in plant height, morphological characteristics and biomass production Trait

Method

Plant height Plant height growth rate Leaf length Leaf width Leaf area Leaf angle

Maximum of root length Number of roots The aboveground fresh biomass

Measured from the base of the seedling to the tip of the longest leaf Calculated daily average increase in plant height Distance from the junction of the blade and leaf sheath to the tip of the blade Measured at the widest portion of the blade Estimated as the product of length and width Measured angle with protractor between the line of the pulvinus with leaf tip and the stem Length of the longest secondary adventitious root measured from collar to the tip of root system Number of secondary adventitious roots Weight of culms and all associated leaf structures after cutting the seedlings at ground level

by measuring the absorbance at 663 nm (Chla), 645 (Chlb), and 470 nm (Car). Pigment content was expressed in milligrams in per gram of fresh leaf, according to the equation:60 ( ) Chla = 12.72D663 − 2.59D645 × V∕1000W ( ) Chlb = 22.88D645 − 4.67D663 × V∕1000W ( ) Car = 4.08D470 − 0.01Chla − 0.47Chlb × V∕1000W where V is the volume of the extract (mL) and W is the leaf fresh weight (g). D indicates the absorbance value obtained at the indicated wavelength. 2.2.4 Photosynthetic parameters Net photosynthetic rate (Pn), stomatal conductance (cond), intercellular CO2 concentration (Ci) and transpiration rate (Tr) were measured using a portable photosynthesis Instrument (LI-6400; LI-COR Biosciences, Lincoln, NE, USA) at 09.30 to 11.00 hours on a sunny day. Each single seedling of each pot was measured.

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2.2.5 Chlorophyll fluorescence kinetic parameters Chlorophyll fluorescence kinetic parameters were determined with a Handy-PEA fluorometer (Plant Efficiency Analyzer; Hansatech Instruments Ltd., King’s Lynn, UK) as described by Strasser and Govindjee,61 and Strasser et al.62 Prior to measuring, individuals were pre-adapted in the dark for 30 min and then exposed to a wavelength of 650 nm at a light intensity of 3500 μmol m−2 s−1 , with a red induction time of 1 s. The raw data of chlorophyll fluorescence parameters was processed with the PEA Plus software provided with the instrument and Biolyzer 4HP (Fluoromatics Software, Geneva, Switzerland). The fluorescence OJIP transients were analysed using the JIP-test.62 The JIP-test defines the maximal (subscript ‘o’) energy

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fluxes in the energy cascade for the events of absorption (ABS), trapping (TRo ), electron transport (ETo ), dissipation (DIo ), and excited leaf cross-section (CS). These parameters in this experiment were as follows: when t = tFm , PI(abs) : a comprehensive performance index on absorption basis. ABS/CSm: absorption flux per excited cross section TRo /CSm: trapped energy flux per excited cross section ETo /CSm: electron transport flux per excited cross section RC/CSm: density of the reaction centres (QA reducing reaction centres) per excited cross section • DIo /CSm: dissipated energy flux per excited cross section

• • • •

2.3 Data analyses Data was analysed by the ANOVA procedure and means were separated using the Duncan’s multiple range test (P < 0.05). Additionally, Pearson correlations, with a two-tailed significance test (P < 0.05), were used to analyse the correlations between genetic diversity indexes of the weedy rice biotypes and the measured indexes of the biotypes. All the statistical analyses were carried out using the SPSS (17.0, SPSS Inc. Chicago, IL, USA) software package.

3

RESULTS

3.1 Seed characteristics of weedy and cultivated rice WRLN004, WRGD008 and the rest of the weedy rice had black, straw and brown hulls, respectively (Table 2). Both rice cultivars, ZD-8 and SY-63 had straw hulls. The caryopses of all weedy rices had red or reddish brown pericarp, while that of the two cultivated rice cultivars was white. The seed shape (seed length/width ratio) of WRGD008 and SY-63 was significantly greater than that of the other weedy rice biotypes while cultivated ZD-8 had the lowest ratio. Grain thickness of ZD-8 was greatest, followed by WRJS023. The rest of the rice materials were similar in grain thickness. The two rice cultivars had greater thousand kernel weight (TKW) than all weedy rice biotypes, which varied among themselves with the following significant decreasing order: WRJS013, WRJS023, WRLN004, WRHA010, WRGD008 and WRLN003 (Table 2). 3.2 Seedling emergence All weedy rice biotypes emerged 2–3 days earlier than cultivated rice (Fig. 1). The biotypes from Jiangsu emerged at 3 DAS, a day later than the rest that emerged at 2 DAS. Both rice cultivars emerged at 5 DAS. Weedy rice biotypes continued emerging for eight to nine days except for WRLN004 that completed emergence earlier. Overall, emergence of weedy and cultivated rices was more than 95% without significant difference among them. Altogether WRJS013, WRJS023 and cultivated rices completed emergence at 12 DAS, the rest of the weedy rice biotypes did so at 10 DAS except for WRLN004, which did not further emerge beyond 6 DAS. Therefore, all weedy rice biotypes except for WRLN004 emerged earlier, continued emerging for a longer period and completed emergence at the same time or earlier than cultivated rice. WRLN004 was very early, completing emergence in half the time required by cultivated rice (6 DAS). 3.3 Plant height, morphological characteristics and biomass Weedy rices were taller than cultivated rice at the three evaluation dates, except for WRGD008 that at 12 DAS was identical to SY-63 yet taller than ZD-8, which was the shortest rice at

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Enhanced photosynthesis endows seedling growth vigour

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Table 2. Comparison of grain characteristics among the various biotypes of weedy rice and cultivated rice Biotype or cultivar

Hull colour

Pericarp colour

SY-63 ZD-8 WRJS013 WRJS023 WRHA010 WRGD008 WRLN003 WRLN004

Straw Straw Brown Brown Brown Straw Brown Black

White White Red Red Red Red Red Reddish brown

Grain shape

Grain thickness (cm)

2.79b 2.00d 2.42c 2.43c 2.37c 3.10a 2.49c 2.51c

0.20c 0.24a 0.20c 0.21b 0.20c 0.20c 0.19c 0.19c

Thousand kernel weight (g) 29.65a 28.27b 25.10c 24.35d 23.17f 22.53g 20.00h 23.72e

Mean values within a column followed by the same letter are not significantly different according to Duncan’s Multiple Range Test (P < 0.05).

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c

c

a

Emergence onset a

Days(d)

12

b

Continuing emergence b

b

10 8 6

a

d

a b

4

b

c

c

c

c

2 0

SY-63

ZD-8

WRJS013 WRJS023 WRHA010 WRGD008 WRLN003 WRLN004

Cultivar rice and weedy rice

Figure 1. Comparison of seedling emergence onset and time to completion for cultivated and weedy rices. Columns (onset germination times and durations) followed by the same letter do not differ according to a Duncan’s multiple range test (P < 0.05).

this earliest time (Fig. 2). Variability in height among weedy rice biotypes decreased as the seedlings became older with all biotypes reaching a similar height at 24 DAS. Interestingly, WRGD008 that was shortest at 12 DAS had become one of the tallest 6 days later and remained among the tallest at 24 DAS. During the evaluation period, WRJS023, WRHA010 and WRGD008 increased in height at a daily rate of up to 1.68–1.69 cm; WRJS013, WRLN004 and WRLN003 grew taller at a rate of 1.55, 1.35 and 1.28 cm day−1 , respectively. The cultivars grew at 1.18 cm day−1 or less. Length and width of the top second leaf varied substantially among the rice accessions (Table 3). Weedy WRLN004 and cultivated SY-63 had the longest top second leaf while cultivated ZD-8 had the shortest being one third in length of that of WRLN004. There was less variation in width, ZD-8 also having the narrowest leaf. This combination in ZD-8 determined that this cultivar had the lowest leaf area while WRLN004 and SY-63 together with WRJS013 had the highest. The leaf angle of weedy rice biotypes was greater than that of both cultivars. All weedy biotypes were similar in developing longer roots. Five out of six weedy rice biotypes also produced more numerous secondary adventitious roots. Weedy biotypes also produced more above-ground fresh biomass that cultivated rices.

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3.6 Chlorophyll fluorescence kinetics The comprehensive performance index, index PI (abs) that quantifies the overall photosynthetic activity of PSII, was higher in weedy rice biotypes than cultivars by approximately 1.5–2.6 and 1.2–2.1 times compared to ZD-8 and SY-63, respectively (Fig. 4). The density of active reaction centres per excited cross section (RC/CSm), trapped energy flux per excited cross section (TRo /CSm), the absorption flux per excited cross section (ABS/CSm), and electron transport flux per excited cross section (ETo /CSm) of the six weedy rice biotypes were also significantly higher than those of ZD-8 and SY-63. Dissipated energy flux per excited cross section (DIo /CSm) of the weedy rices was lower than that of the cultivars with the exception of WRGD008 and WRLN003 that had similar values to SY-63. The ABS/CSm of weedy rice was 14–25% higher than that of ZD-8 and SY-63. The TRo /CSm of weedy rice was 12–26% higher than ZD-8 and SY-63. Finally, the ETo /CSm of weedy rice was 13–40% higher than the ZD-8, and 4–29% higher than SY-63. Compared to cultivars, weedy rices have a higher probability of absorption flux by pigment antennae, trapping flux by reaction centres, and the trapped exciton movement in photosystem II (PSII) electron transport chain. Thus weedy rice has a higher overall photosynthetic activity of PSII. This is well in agreement with our findings of higher concentration of photosynthetic pigments and the net photosynthetic rate in weedy than cultivated rices. 3.7 Correlation analysis between various traits with photosynthetic pigment content, photosynthesis efficiency and chlorophyll fluorescence Correlation analysis among the various traits was made to comparatively analyse the growth advantage determining the superior competitive characteristics of weedy rice seedlings (Table 5).

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3.4 Photosynthetic pigment content The pigment content of all weedy rice biotypes was higher than that of the two cultivars, which were similar to each other (Fig. 3). The chlorophyll a + b content of weedy rice biotypes was 7–25% higher than that of SY-63 and 14–33% higher than that of ZD-8. Similarly, the carotenoid content of the six weedy rice biotypes was 10–31% and 6–27% higher than those of ZD-8 and SY-63, respectively.

3.5 Photosynthetic parameters The net photosynthetic rate of six weedy rice biotypes was 20–60% and 8–43% higher (P < 0.05) than that of rice cultivars ZD-8 and SY-63, respectively (Table 4). Among weedy rice biotypes, WRJS013 and WRJS023 exhibited the highest net photosynthetic rates. Cultivated rice ZD-8 and SY-63 had a lower stomatal conductance than all weedy rices; the biotypes WRJS013 and WRJS023 doubled the stomatal conductance of the crop plants. All weedy rices also had higher intercellular CO2 concentrations and transpiration rates than ZD-8. The majority of them also exhibited higher intercellular CO2 concentrations than SY-63, except for WRLN003 that shared a similar one with the cultivar. Three of the weedy rices had higher transpiration rate than SY-63.

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SY-63

40 a a a

Plant height (cm)

35 a

30

a a a a

b 25

a a

ZD-8

a

WRJS013 WRJS023

b

WRHA010

b

c c

WRGD008 20

a a

a b b

15 c

WRLN003 WRLN004

c

d

10 5 0

12 DAS

18 DAS

24 DAS

Day after sowing (DAS) Figure 2. Plant height of cultivated and weedy rices at three different times after sowing. Columns (plant height) labelled with the same letter within an evaluation date do not differ according to a Duncan’s multiple range test (P < 0.05).

Table 3. Foliar and root characteristics and above-ground biomass production of weedy and cultivated rice seedlings Biotype or cultivar

LL (cm)

LW (cm)

SY-63 ZD-8 WRJS013 WRJS023 WRHA010 WRGD008 WRLN003 WRLN004

12.90a 4.67d 10.35b 9.75b 10.48b 9.93b 7.70c 14.33a

0.40a 0.20d 0.43a 0.40a 0.36ab 0.28c 0.28c 0.30bc

LAG (∘ )

LAR (cm2 ) 3.87a 0.70d 3.29ab 2.93b 2.79b 2.09c 1.57c 3.23ab

MRL (cm)

28.75cd 23.75d 33.8bcd 35.00bc 42.00b 36.00bc 62.50a 65.00a

NSAR

9.30e 10.63e 16.15a 15.48ab 14.00c 12.8d 12.03d 15.03b

6.33d 5.75d 10.75a 10.25a 9.5ab 8.25bc 7.25cd 9.25ab

AFB (g) 0.11c 0.11c 0.16a 0.16a 0.13b 0.13b 0.12bc 0.15a

Different letters within a column indicate a significant difference for the characteristic among the various biotypes of weedy rice and cultivated rice based on Duncan’s Multiple Range Test (P < 0.05). LL, leaf length; LW, leaf width; LAR, leaf area; LAG, leaf angle; MRL, maximum of root length; NSAR, number of secondary adventitious roots; AFB, above-ground fresh biomass.

Pigment content(mg/g)

2.5 2 de

1.5

ef

ab bc a cd abc cd

SY-63

a ab bcd cd bc de

3

ZD-8 WRJS013

f

WRJS023 WRHA010 WRGD008

e

1 ef f

ab bcd cd a de bc ef f

bcd cd a b de bc

WRLN003 WRLN004

0.5 0

Chla

Chlb

Chla+b

Car

Pigment species

1414

Figure 3. Content of photosynthetic pigments of the top second leaf weedy and cultivated rice accessions. Columns representing rice (weedy and cultivated) accessions labelled with the same letter do not differ in the respective pigment (Chla, Chlb, Chla + b, Car) content according to a Duncan’s multiple range test (P < 0.05). Chl, chlorophyll; Car, carotenoids.

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Table 4. Photosynthetic parameters of various biotypes of weedy rice and cultivated rice Cond Ci Biotype or Pn cultivar (μmol m−2 s−1 ) (mmol · m−2 · s−1 ) (μmol mol−1 ) SY-63 ZD-8 WRJS013 WRJS023 WRHA010 WRGD008 WRLN003 WRLN004

20.18e 18.13f 28.9a 28.31a 24.99c 24.55c 21.83d 26.50b

0.28fg 0.25g 0.56a 0.49b 0.42c 0.35de 0.31ef 0.37cd

239.55d 208.25e 293.00a 277.25b 256.55c 263.00c 245.75d 261.00c

Tr 9.56c 7.68d 12.75a 12.35ab 11.46abc 10.70bc 9.63c 12.55ab

Values within columns followed by the same letter do not differ according to Duncan’s Multiple Range Test (P < 0.05). Pn, net photosynthetic rate; Cond, stomatal conductance; Ci, intercellular CO2 concentration; Tr, transpiration rate.

DIo/CSm

PI(abs) 30 25 20 15 10 5 0

RC/CSm

SY-63 ZD-8

ABS/CSm

WRJS013 WRJS023 WRHA010 WRGD008 WRLN003 WRLN004

ETo/CSm

TRo/CSm

Figure 4. Comparison of chlorophyll fluorescence kinetic parameters among the various biotypes of weedy rice and cultivated rice.

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4

DISCUSSION

Weedy rice emerged earlier and its seedlings grew faster, had superior morphological traits, and displayed enhanced photosynthetic physiological capacity compared to cultivated rice. Those remarkable characteristics should contribute to its superior competitive ability with the crop. Although the weedy biotypes characterised in this study originate from contrasting latitudes, they all exhibited traits that explain their competitive advantage over the crop demonstrated in a previous study.8 There was no coincidence in the patterns of emergence and its duration or the height and biomass of the rice seedlings with the size and weight of the seed that originated them or the sub-species to which they belonged. There is ample discussion as well as contradictory results regarding a possible survival, growth and competitive advantage associated with seed size among and within species.63 – 65 Interestingly, although there was variability in height among all weedy rice biotypes at 24 DAS, differences were not large enough to be significant but attained height closely followed initial seed weight. Conversely, the cultivars on average had the heaviest seed but only attained about 70% the maximum above-ground fresh biomass of weedy rices. In a study by Li and Rutger,66 both rice kernel weight and earliness highly correlated with cool-temperature height (seedling vigour) of 14-day-old seedlings but poorly with mature plant height. Once a seedling emerges, the subsequent growth of the coleoptile and succeeding leaves largely depends on the seed reserves; about 60% of the seed weight is allocated to new organs (growth efficiency) until the seedling turns into an autotrophic plant at the four-leaf stage.67 Among 36 cultivars, seedlings arising from seeds having heavier embryos and endosperms developed larger leaf areas and biomass in javanica but not in japonica or indica rice.43 Seed size and seedling characteristics are controlled by polygenes and there is an apparent genetic association between seed size and the length of the second seedling leaf according to a study using QTLs.49 In the closely related Poaceae, Zizania palustris seed size determined seedling height but not the rate of emergence.68 Obviously, weedy rice seedling vigour was not determined by seed weight compared to cultivated rice. It could be that intrinsic genetic mechanisms endowed enhanced vigour to weedy rice seedling compared to cultivated rice. Environmental factors (depth of seed in the soil and soil quality) and intrinsic rate of germination determine the time to emergence of a seedling.69 Several previous experiments have addressed emergence behaviour of weedy rice. Vidotto and Ferrero70 found that the emergence of weedy rice decreased with the depth of seed burial in saturated soil and by the presence of a water layer on the soil surface. Similarly, Chauhan71 found that flooding depth ranging from 0 to 8 cm had little or no effect on seedling emergence of several weedy rice accessions sown on the soil surface but decreased it when seeds were sown at 1 cm deep into the soil. Gealy et al.4 demonstrated that emergence of weedy rice under dry-seeded culture was influenced by weedy rice ecotype, seeding depth and soil type. In the present study, environmental factors including soil type and water content were uniform and mother-plant effects can be ruled out since the seed used for

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Generally, there was a highly significant or significant positive correlation (P < 0.01 or P < 0.05) between photosynthetic pigment content or photosynthesis efficiency and the majority of traits. This implied that plants having greater genetic diversity index, plant height and growth rate, larger leaf area, longer root length, increased root number, and greater above-ground fresh biomass also contained more photosynthetic pigments and were photosynthetically more efficient. But negative correlation between some parameters of photosynthetic pigment content or photosynthesis efficiency with thousand kernel weight (TKW) and grain thickness occurred. A highly significant or significant positive correlation between the majority of traits with parameters of chlorophyll fluorescence kinetics (ABS/CSm, ETo /CSm, TRo /CSm, RC/CSm) was observed, except for TKW and grain thickness. TKW highly negatively correlated (P < 0.01) with ABS/CSm and TRo /CSm, and did not correlate with ETo /CSm, RC/CSm. GT negatively correlated with ABS/CSm, TRo /CSm, ETo /CSm and RC/CSm. This implied that plants with greater genetic diversity index, plant height and growth rate, larger leaf area, longer root length, increased root number, and greater above-ground fresh biomass also had higher ABS/CSm, ETo /CSm, TRo /CSm, and RC/CSm. However, plants with higher thousand kernel weight or grain thickness had less ABS/CSm and TRo /CSm or ABS/CSm, TRo /CSm, ETo /CSm and RC/CSm, respectively. Meanwhile, highly significant or

significant negative correlation between most traits with DIo /CSm was observed indicating that plants with greater genetic diversity index, plant height at 24 DAS, growth rate, leaf area, longer root length, increased root number, and greater above-ground fresh biomass had lower DIo /CSm.

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Table 5. Correlation analysis between photosynthetic pigment content, photosynthesis efficiency and chlorophyll fluorescence with traits of weedy rice biotypes and rice cultivars Photosynthetic pigment content Trait

Chla

GDI 0.481** GT −0.442* GS 0.087 TKW −0.421* SED 0.184 H12 0.370* H18 0.428* H24 0.724** GR 0.652** LAR 0.521** LAG 0.223 RL 0.575** RN 0.839** AFB 0.787**

Chlb 0.455** −0.420* 0.069 −0.409* 0.191 0.343 0.406* 0.719** 0.627** 0.489** 0.207 0.573** 0.836** 0.765**

Car

Photosynthesis efficiency Pn

Cond

Ci

Chlorophyll fluorescence Tr

0.442* 0.550** 0.519** 0.495** 0.431** −0.438* −0.357* −0.418* −0.198 −0.495** 0.082 0.035 0.139 −0.047 0.320 −0.362* −0.405* −0.223 −0.381* −0.303 0.144 0.206 −0.111 0.080 0.292 0.276 0.367* 0.111 0.320 0.439* 0.386* 0.477** 0.263 0.392* 0.389* 0.683** 0.779** 0.687** 0.761** 0.635** 0.630** 0.744** 0.674** 0.705** 0.570** 0.477** 0.486** 0.373* 0.542** 0.516** 0.168 0.200 0.016 0.169 0.220 0.611** 0.614** 0.545** 0.539** 0.487** 0.845** 0.862** 0.756** 0.760** 0.730** 0.801** 0.839** 0.790** 0.791** 0.633**

ABS/CSm

ETo/CSm

0.557** −0.477** 0.147 −0.654** 0.353* 0.545** 0.379* 0.853** 0.750** 0.303 0.392* 0.617** 0.816** 0.810**

0.444* −0.507** 0.130 −0.321 0.151 0.303 0.593** 0.755** 0.635** 0.546** 0.207 0.606** 0.840** 0.862**

TRo/CSm 0.551** −0.427* 0.062 −0.570** 0.311 0.471** 0.127 0.836** 0.746** 0.348 0.333 0.630** 0.838** 0.835**

RC/CSm

DIo/CSm

0.332 −0.463** 0.102 −0.127 −0.064 0.006 −0.118 0.594** 0.534** 0.432* −0.017 0.547** 0.751** 0.779**

−0.372* 0.185 0.094 0.098 0.223 −0.019 −0.118 −0.585** −0.568** −0.452** 0.081 −0.507** −0.758** −0.774**

GDI, genetic diversity index; GT, grain thickness; GS, grain shape; TKW, thousand kernel weight; SED, seedling emergence days earlier than cultivated rice time; H12, plant height at 12 DAS; H18, plant Height at 18 DAS; H24, plant height at 24DAS ; GR, growth rate; LAR, leaf area; LAG, leaf angle; RL, root length; RN, root number; AFB, aboveground fresh biomass; Chla, chlorophyll a; Chlb, chlorophyll b; Car, carotenoids; Pn, net photosynthetic rate; Cond, stomatal conductance; Ci, intercellular CO2 concentration; Tr, transpiration rate; ABS/CSm, absorption flux per excited cross section; ETo/CSm, electron transport flux per excited cross section; TRo/CSm, trapped energy flux per excited cross section; RC/CSm, density of the reaction centers; DIo/CSm, dissipated energy flux per excited cross section. *Correlation is significant at the 0.05 level (two-tailed). **Correlation is significant at the 0.01 level (two-tailed).

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establishing the experiments was also produced under uniform conditions. Therefore, the differential emergence among weedy rice and cultivated rice was determined by the intrinsic rate of germination. The six weedy rice biotypes (two japonica and four indica) began emerging 2–3 days earlier than both the japonica and indica cultivars. Similar results were found by Sánchez-Olquín et al.34 among Costa Rican indica weedy and cultivated rices that although similar in their % of total emergence differed in earliness of emergence, with 38% of the weedy rice morphotypes emerging significantly earlier than cultivars. Although the intrinsic reason for earlier emergence of weedy rice than cultivars has not been reported until now, Chung72 found weedy rice germplasm that had superior abilities to emerge from greater depths than cultivated rices, and that coleoptile and mesocotyl lengths were highly positively correlated with the emergence rate. Therefore the elongation of coleoptile and mesocotyl played an important role in seedling emergence of weedy rice. Early-emerging plants capture space and thus have greater access to light and nutrients than late-emerging ones.73 Thus, individual fates are already largely determined at the time of emergence.69 Eckersten et al.74 found spring barley emerged 8 and 26 days later than weeds and this late emergence resulted in a decrease of above-ground crop biomass coverage by 50% and 10%, respectively. From an agroecological perspective, it is important to emphasise that weedy rice began emerging earlier and completed emergence at the same time or faster than the crop having therefore a better opportunity to become established, which is a determinant for the final outcome of competition. In the two cases where there was coincidence in time of completion of emergence between weedy and cultivated rice, i.e. for the biotypes WRJS013 and WRJS023 (Fig. 1), at such time weedy rice seedlings had a significant advantage in plant height over the crop plants that remained throughout the seedling stage (Fig. 2).

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Plant height is directly linked to plant competitiveness, thus taller plants are more competitive than shorter ones because of better light interception, and a direct association with photosynthetic activity of the plant.75 – 81 During the observation period, seedlings of weedy rice increased in height at a daily rate of up to 1.69–1.28 cm, whereas that of the cultivars was 1.18 cm or less. Sánchez-Olquín et al.34 also found that weedy rice increased in height 10–30 cm every 2 weeks. In contrast, the increase in height for commercial rice varieties was considerably lower (8–14 cm) during the same period. Ahmed et al.35 reported that plant height of several weedy rice morphotypes in Malaysia was significantly higher compared to the commercial varieties at every growth stage. Leaves are the major organs of photosynthesis in vascular plants. Leaf area and leaf angle are also linked to competitiveness. Leaf area is often associated with the potential light interception. Leaf area of the six weedy rice biotypes was significantly greater than that of ZD-8 but lower than that of the other cultivar (SY-63). Plants with larger leaf area often had a competitive advantage compared with those with smaller leaf area.82 – 84 Leaf angle influences the ability of plants to intercept light.85,86 Species with wider leaf angles had greater whole-day light interception than narrower species, except in winter.87 The leaf angle of the six weedy rice biotypes was larger than that of both cultivars implying that weedy rice seedlings could intercept more light than those of cultivated rice. Individual plant size is an important factor determining the competitiveness in grass weeds such as Echinochloa crus-galli.69 Namuco et al.88 demonstrated that rice biomass at 28 days was correlated with grain yield in competition with weeds. The above-ground fresh biomass of six weedy rice biotypes was also significantly greater than that of the two cultivars at 24 DAS. It

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the combined action of their antenna size, active reaction centres and quantum yield for electron transfer beyond QA . This further confirmed that weedy rices possess significantly higher net photosynthetic rate than cultivars. Thus, it is concluded that development of high photosynthetic capacity plays an important role for weedy rice seedling establishment and its superior competitive ability against cultivated rice. Correlation analysis between various traits with photosynthetic pigment content, photosynthesis efficiency and chlorophyll fluorescence showed that those traits associated with seedling vigour (greater plant height and growth rate, leaf area, root number and length, above-ground fresh biomass) were highly correlated with photosynthetic pigment content and photosynthesis capacity. Therefore an increased photosynthetic pigment content and stronger photosynthesis capacity resulted in greater seedling vigour in weedy rice. However, TKW and time of seedling emergence were negatively or not correlated with photosynthetic pigment content and photosynthesis efficiency, respectively. This implies that lighter seed and earlier seeding emergence of weedy rice did not confer higher photosynthesis. Furthermore, the strong positive correlation between genetic diversity index with photosynthetic pigment content and higher photosynthesis capacity probably determines the increased seedling vigour of weedy rice. Seedling vigour of weedy rice consequently endows its strong field competiveness compared to cultivars, which was already demonstrated by Dai et al.8 with the same biotypes and the ZD-8 cultivar. However, other agroecological aspects interact in determining the final outcome of competition. The level of weedy rice infestation in the field (as predicted from changes in the experimental replacement proportion in a competition study) and germination time affect the yield of the crop (planted at a fixed density) differentially. Thus with increased proportion, weedy rice demonstrated increased suppressive effects on seedling height of cultivated rice 45 DAS due to rapid seedling growth. WRHA010 and WRGD008 (both indica) and WRLN003 and WRLN004 (the two japonica weedy rices included in the study) were more competitive than WRJS013 and WRJS023 (medium genetic diversity, highest photosynthetic parameters) at 45 DAS, while WRHA010, WRGD008, WRJS013 and WRJS023 were more competitive than WRLN003 and WRLN004 at 85 DAS. Overall, WRHA010 and WRGD008 weedy rice (with greatest genetic diversity) had the greatest negative effect on the growth of cultivated rice. Though competitive interactions between weedy and cultivated rice are very complex, vigorous weedy rice seedling establishing early is at a great advantage to outcompete cultivated rice.

5

CONCLUSION

Weedy rice had advantages in seedling emergence time, plant height, root number and length, leaf area and angle, photosynthetic capacity, growth rate and above-ground biomass, compared to cultivated rice. The competitive advantage of weedy rice seedlings is closely related to seedling emergence time, plant height, growth potential, genetic diversity index and photosynthetic capacity. Obviously, early establishment of weedy rice and higher photosynthetic potential at the seedling stage led to strong competitive superiority in space, time and physiology over cultivated rice. Practical agronomic implications of this study emphasise the importance of controlling weedy rice early while it is still at the seedling stage.

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implied that weedy rice could be more competitive and potentially produce higher grain yield than cultivated rice. The number of root tips bearing root hairs that act as major water and nutrition uptake sites, is also indicative of competitive ability.89 Five of the six weedy rice biotypes had more roots than both cultivars. Increased root number favours nutrient uptake and contributes to greater biomass. Burgos et al.32 found that weedy rice takes up more N, and has higher N use efficiency for biomass production than cultivated rice. Furthermore, Sales et al.90 demonstrated that weedy rice had more root tips than cultivated rice, and had greater N and sucrose tissue concentrations at N-deficient conditions compared with cultivated rice. Therefore seedlings of weedy rice have a competitive advantage over those of cultivated rice by growing taller and faster, and having a massive root system, which helps depriving cultivated rice of necessary nutrients. Photosynthetic pigments on the chloroplast thylakoid membrane absorb visible light, and transfer it to chlorophyll molecules. Hence, leaf pigment content is an important indicator of plant photosynthetic capacity. Chlorophyll a favours absorption of long-wave light, chlorophyll b does it for short-wave light, and carotenoids absorb the other-wave light and, being endogenous antioxidants, protect chlorophyll from photodynamic injury.91,92 Weedy rice biotypes contained more photosynthetic pigments than cultivated rice, which obviously conferred then a great photosynthetic advantage over the crop. Photosynthesis is the plant basic physiological processes determining plant growth and development.50 Net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, and transpiration rate indicators are important parameters describing the capacity of a plant to carry out photosynthesis.93 These photosynthetic parameters were always significantly higher in weedy rice than in the ZD-8 cultivar, and in most cases than those of SY-63. Hence, weedy rice had stronger photosynthetic capacity than cultivated rice. Higher photosynthetic capacity of weedy rice led it to accumulate photosynthates that promoted its fast growth thus giving it competitive advantage over cultivated rice.94,95 The chlorophyll fluorescence rise kinetics combining JIP-test is an excellent tool in the investigation of plant photosynthetic physiological states because it is nondestructive, precise and quick.60,61 The detailed metabolic process as well as the structure and function status of the photosynthetic apparatus can be quantified by different JIP-test parameters. ABS/CSm refers the absorption flux per excited leaf cross-section, which can be taken as a measure for an average antenna size or chlorophyll concentration. TRo /CSm expresses the trapped energy flux per excited leaf cross-section, which reflects the specific rate of the exciton trapped by open RCs per excited leaf cross-section.61 Since weedy rices exhibit a higher ABS/CSm and TRo /CSm relative to cultivars, it is likely that a bigger antenna or chlorophyll concentration and more stable architecture of the antenna complexes exists in the photosystem II of weedy rice. High density of PSII active reaction centres (RC/CSm) was also observed in the weedy biotypes. The more effective energy absorption, trapping and transfer from antennae to reaction centres certainly leads to a high efficiency of PSII electron transport (ETo /CSm), followed by a low energy dissipation (DIo /CS) in the weedy rices. The performance index (PIABS ) combines the responses of PSII due to the photochemical and non-photochemical properties as well as those due to the density of active reaction centres per chlorophyll absorption, thus expressing the overall photosynthetic activity of PSII.62 Here, a stronger overall photosynthetic activity in weedy rices should result from

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ACKNOWLEDGEMENTS This research was financially supported by the Doctoral Program of Higher Education of the Ministry of Education (20130097130006), China Transgenic Organism Research and Commercialization Project (2016ZX08011-001), PAPD and the 111 Project. The authors thank Ms Rui Liu and Ms Lili Wu for their assistance in these experiments and proof reading of the article.

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