Agricultural Reviews, 38(3) 2017 : 209-215 AGRICULTURAL RESEARCH COMMUNICATION CENTRE

Print ISSN:0253-1496 / Online ISSN:0976-0539 [Link]

Physiological and molecular response to low light intensity in rice: A review

Suvendhu S. Dutta, Wricha Tyagi1 and Mayank Rai*
School of Crop Improvement, College of Post-Graduate Studies,
Central Agricultural University (Imphal), Umiam-793 103, Meghalaya, India.
Received: 19-12-2016 Accepted: 18-07-2017 DOI:10.18805/ag.v38i03.8980
ABSTRACT
Rice being the staple food of the world, its production is of immense importance. But rice productivity is dependent on
appropriate light intensity, among other factors. This review focuses on morphological, physiological and biochemical the
effects of low light on rice yield and quality. An attempt has been made to give the progress made in this important area of
rice research along with future research directions that can be taken to improve rice grain yield and quality under low light
stress.
Key words: Chlorophyll, Low light, Rice.

Rice (Oryza sativa L.) is known as “Global Grain” stage, reduction in spikelet number; increased spikelet
and provides staple food for more than half of the world’s sterility and reduced dry matter production are commonly
population. Among rice growing countries in the world, India observed. As compared to normal light (1000-1200 MJ m-
has the largest area under rice crop and ranks second in 2 -1
d ), photosynthetic rates are considerably reduced under
production next to China. Eastern and north eastern regions low light intensity (410-415 MJ m-2d-1).
of India accounts for about 60% of total rice-cropped area, With the increase in global warming the occurrence
but contribute only 48% of the total production. More than of overcast, rainy sky and low light intensity has become a
half of the area (55%) under rice cultivation is rain-fed and prevalent problem. It is now known that low light stress
80% of this rain-fed rice area lies in eastern and NE India. affects every aspect of vegetative growth (plant height, tiller
Apart from being vulnerable to the vagaries of monsoon and number, root growth, stoma regulation and chlorophyll
other biotic and abiotic stresses, occurrence of low light development), photosynthesis, dry matter accumulation and
intensity is also a prevalent problem. Among the eastern partition, and yield and quality of rice (Xiu et al., 2013).
Indian states, hill regions of north eastern region (NEHR)
experience the cloudiest conditions (Adhya et al., 2008). Relation of temperature with light intensity: It has been
suggested that light intensity and temperature have important
Light is a critical natural resource, which controls
relationship. Higher temperatures (35-42°C) in association
morphogenesis and production in plants. It has a major role
with either high or low light intensity exert a negative
in photosynthesis, photoperiodism, and photonasty. In fact,
influence on crop growth and productivity. Also low
agriculture can be defined as the exploitation of solar
temperatures (25-30°C) with lower light intensity (150-200
radiation with the help of water and nutrients (Fageria, 2013).
cal) exert a negative effect. But moderate temperatures (28-
Low light intensity is a critical abiotic stress that reduces
32°C) and light intensity (350- 450 cal) are very favourable
rice yield and quality. Since the growth and yield of rice
for higher productivity. This combination is very rare, but
crop are significantly affected by low light stress, the
when it occurs, it gives higher yields. Thus, the magnitude
molecular mechanism of low light adaptation/tolerance is
of the problem of low light intensity naturally depends on
of vital interest. Rice plant on an average requires about
1500 bright sunshine (BSS) hours for the period from all these factors that vary by latitude, altitude, and proximity
transplanting to maturity. But in Eastern and NEHR of India, to seas, landslides and rain forests (Venkateswarlu and
only about 800-900 BSS hours of light is received during Visperas, 1987).
the months of August to December. This hampers the Response of photoperiodism with light intensity: Many
physiological efficiency, and ultimately the productivity of flowering plants use phytochromes to regulate the time of
rice. Because, solar radiation in tropics is one of the major flowering, and to set circadian rhythm (Taiz and Zeiger,
climatic factors limiting grain yield in rice (Barmudoi and 2010). The intensity of light is an indication of the strength
Bharali, 2016), low light (less than 1000 MJ m-2d-1), affects of a light source at a particular wavelength which is important
all the stages of rice growth. Under low light conditions; in determining the flowering process in many plants. Baloch
high tiller mortality at vegetative stage and at reproductive et al. (2012) reported that many long day ornamental plants
*Corresponding author’s e-mail: [Link]@[Link]
210 AGRICULTURAL REVIEWS
respond better to more intense light sources. This intensity ~20% due to low light intensity. The synthesis and
of irradiance varies from plant to plant, such as flowering degradation of the photosynthetic pigments are associated
plants require 6,000-10,000 lux (74-124 mol.m -2.s-1), with the plants adaptability to different environments. The
flowering bulbs need 500-1,000 lux (6-12 mol.m-2.s-1) and chlorophylls are usually synthesized and photo-oxidized in
most foliage plants need 1,000-6,000 lux (12-74 mol.m- the presence of light (Zervoudakis et al., 2012).
2 -1
.s ) light irradiance (Thomas and Vince-Prue, 1997). The Accumulation, translocation, distribution of dry matter
leaf development and flowering rate in cyclamen is governed and nitrogen with response to low light intensity: It has
by light intensity instead of photoperiod (Baloch et al., 2012). been reported that a 10-21% reduction in total dry matter of
Morphological and photosynthetic response of rice plant the crop occurs at panicle initiation, flowering and harvest
under low light intensity: Leaf morphology affects stages under low light (as compared to normal white light
photosynthetic efficiency. The leaves grown in low irradiance (Barmudoi and Bharali, 2016). A wide gap between spikelet
have lower rates of photosynthesis due to a low content of number and number of filled grains was reported during the
photosynthetic component per unit leaf area. However, wet season due to the poor supply of carbohydrates from the
changes also occur at the single chloroplast level: the ratio source leaf. Under low light conditions, the total dry weight
of PSII to PSI has been shown to vary according to irradiance (shoots + roots) in rice plants increases suggesting that the
level (Murchie and Horton, 1998; Yamazaki et al., 1999). decrease in dry matter in roots is more than that of shoots
Plants grown under low light conditions have more peripheral (Liu et al., 2014). Similarly, Yamamoto et al. (1995) also
light-harvesting complexes per PSII reaction center and a found an increase in dry weight in culm under low light
higher amount of rubisco per unit chlorophyll, and intensity when compared to total shoot (culm + tillers). The
cytochrome b/f complex per unit chlorophyll (Murchie and low light conditions results in less amount of N allocated to
Horton, 1998; Beneragama and Goto, 2010). Liu et al. (2006) panicles as compared to that under natural light (Liu et al.,
observed that the ribulose bisphosphate carboxylase 2014). The source of N under low light intensity shifts
(Rubisco) activity in chloroplasts declines dramatically under towards NH3 to optimize energy available for biosynthesis
low light conditions. The light intensity also alters the rates (Poolman et al., 2013).
of non-photochemical quenching, electron transfer and Oxidative stress, anti-oxidative defense system, starch
quantum yield of PS II (Jiao and Li, 2001). Rice has been accumulation and starch synthesis response with low light
shown to show acclimation according to irradiance level intensity: Low light intensity has a great impact on the
(Murchie et al., 2002). oxidative stress and anti-oxidative defence system. The
Chlorophyll a and b are important pigments which behaviour of tolerant and susceptible genotypes to low light
are involved in the absorption and transmission of solar is considerably different. The low light tolerant genotypes
energy, Wang (2011) reported. Variation in chlorophyll can maintain the scavenging of reactive oxygen species and
content produced in response to low light among varieties the water potential in cells. This helps to minimize the
has been reported (Zhu et al., 2008; Liu et al., 2009). The adverse effects of low light on plant physiological
varieties that are tolerant to low light exhibit higher metabolism, due to the promotion of antioxidative enzyme
chlorophyll b and lower chlorophyll a/b content in their activity and osmotic regulation. Whereas the low light
leaves when subjected to low light for 15 d (Liu et al., 2014). susceptible varieties show cell membrane damage (Liu et
Liu et al. (2009) reported that after being treated by low al., 2012).
light from the transplanting to the booting stages leaf
chlorophyll a and b content during the grain- filling stage is Tian et al. (2006) reported that under low light
markedly enhanced in low light tolerant varieties, whereas condition, starch, amylose and sucrose contents decreased,
the opposite is found in varieties that perform poorly in low but ADP-glucose pyrophosphorylase (ADPGPPase) activity
light. Ren et al. (2002) suggested that tolerant varieties showed a little change. They also found soluble starch
capture as much solar energy as possible under low light synthase activity and granule bound starch synthase activity
conditions through increased leaf area and higher chlorophyll decreased, while soluble starch branching enzyme (SSBE,
b content.. It is also reported that low light negatively affects Q-enzyme) activity and granule bound starch branching
stomatal conductance (fewer stomata are produced per enzyme (GBSBE, Q-enzyme) activity increased. In case of
square millimeter) and results in enhanced concentrations starch debranching enzyme (DBE, R-enzyme), the activity
of intercellular CO2 in rice leaves (Meng et al., 2002; Yang varied with varieties. It is reported that low light during the
et al., 2011). Study by Restrepo and Garcés (2013) showed grain-filling stage results in a decreased supply of
that the leaf chlorophyll content (SPAD readings) was higher carbohydrates to grains as well as a decrease in starch
in rice leaves under low irradiance. Also, at the flowering synthase activity in grains, which directly inhibits grain filling
and grain filling stages, grain yield was reduced by around and enhances the occurrence of chalky rice (Li et al. 2005).
 Volume 38 Issue 3, 2017 211

Spikelet fertility and pollen viability: According to Sridevi major constraints to yield are low grain numbers per panicle
and Chellamuthu (2015), the impaired translocation of in short-duration varieties, high spikelet sterility in medium-
carbohydrates from source to developing grain under duration varieties, and low panicle numbers in long-duration
varieties. Loss in economic yield (12-35%), biological yield
subdued light results in high sterility. Reduced grain yield
(5-29%) and harvest index (7-10%) under low light
under low light intensity is attributed to the cumulative
conditions in comparison to normal light in both pot and
influence of fewer panicles m-2 and grain number panicle-1
field experiments has been reported in winter rice variety
and lower test weight and higher percentage of spikelet
Manoharsali (Barmudoi and Bharali, 2016).
sterility. Under low light conditions at flowering stage,
carbohydrate content, protein synthesis, proline and Rice is cultivated mainly for its edible grains of
cytokinin accumulation decreases and gibberellins and which size and weight are crucial. The study with Nigerian
soluble N in the panicle increases, leading to high spikelet local rice variety, Ofada, revealed that both the grain weight
sterility. As rice is a short day plant, it is subjected to pollen and the economic yield increased under increasing light
sterility, mainly in the later formed florets under low light intensity (Emmanuel and Mary, 2014) In rice plants growing
conditions. The grain development depends mostly on the under low light conditions; from the transplanting to the
contribution of reserve carbohydrates or dry matter booting stages, the yield as well as amylose content increased
production before flowering (Hebbara et al., 2003). It has while the percentage of chalky kernels and protein content
declined (Liu et al., 2014).
been reported that, if the harvest index is low due to poor
partitioning of dry matter to panicle then there is high spikelet Molecular biology of low light intensity tolerance: Shade
sterility (Barmudoi and Bharali, 2016). tolerance refers to the capacity of a given photosynthetic
organism to tolerate low light levels and it is typically
Grain yield and grain quality: The high yield potential is
characterized by a set of morphological and physiological
mostly expressed with adequate solar radiation during the
traits such as decrease in growth rate, light compensation
dry season. Due to the cloudy days with inadequate light
point, dark respiration rate, net photosynthetic rate and
intensity grain yield is comparatively low during the wet chlorophyll a/b ratio, increase in quantum yield, chlorophyll
season. Grain yield correlates positively with solar radiation, content (both per area and per dry mass basis) and
especially during reproductive stage of rice plant. In rice carbohydrate storage together with many other traits
plant grown under low light from the initial heading to (Valladares and Niinemets, 2008). Microarray analysis on
maturity stages, grain yield decreases markedly (up to 55%). rice plants transferred to high light from low light post-leaf
This directly affects decrease in the seed-setting rate and extension revealed a down-regulation of light-harvesting
1000-grain weight (Liu et al., 2014). Singh (2005) reported genes; no change in the expression level of RUBISCO genes
for two rice cultivars, C14-8, and Mansarover, that though and up-regulation of genes involved in photo protection
there was a significant increase in plant height the grain yield Murchie et al. (2005). Covshoff et al. (2013) reported that
and biological yield per plant was decreased under low light light is a key regulator for seedling development of
conditions. Low light stress reduced grain number per panicle monocots; as genome profiling revealed that 18% of the rice
in short duration varieties, increased spikelet sterility in genome is regulated by light in seedlings. The light-regulated
medium duration varieties and decreased panicle number in expression profiles among shoots, roots, and seedlings
long duration varieties. The reduction in grain number per revealed several clusters of genes that were regulated in
panicle by shading of the plants from flowering to harvest is whole seedlings but not in either shoots or roots. In fact,
only due to poor grain filling (Sridevi and Chellamuthu, (Jiao et al., 2005); they also identified common and organ-
2015). Major limitation of higher productivity in the wet specific cis-acting promoter.
season is the natural low light intensity during crop growth. The process of photosynthesis involved several
It is found that same variety shows lower yield in the wet chlorophyll proteins, among which the light harvesting
season than in the dry season. These are attributed mostly to chlorophyll a/b binding (LHC) proteins are crucial. In rice,
reduction in grain number per panicle or per unit land area, there are 17 genomic loci encoding for chlorophyll a/b-
which is a consequence of high spikelet sterility. binding proteins and six loci which encode for early light-
Reproductive and ripening stages of rice are most affected inducible proteins (ELIP1 to ELIP6), two loci for stress-
under low light condition. Low light is commonly enhanced proteins (SEP1 and SEP2), two loci for one-helix
experienced by short- and medium duration rice varieties. proteins (OHP1 and OHP2), and a single loci for light-
But in case of long duration varieties, the low-light stress induced protein 1-like (LIP1-like) (Umate, 2010). Rice LP2
synchronizes with the vegetative lag phase and results in genes promoter is found highly responsive to light (Liu et
considerable tiller mortality and fewer productive panicles al., 2014). By using in silico methods, Bang and Huyen
per m2. During wet season under low light conditions, the (2015) identified a total of 28 genes encoding putative light
212 AGRICULTURAL REVIEWS
harvesting complex (LHC) in coffee (Coffea acenaphora) abundant and versatile microsatellite or SSR markers in the
genome. These coffee LHC genes are classified into many rice genome and information on their physical position in
groups based on phylogeny analysis. Electron flow systems rice genome provide an opportunity to map any gene of
in rice under fluctuating light have also been analyzed interest. These markers have been used in fine mapping and
(Yamori et al., 2016). A targeted proteomics approach to pyramiding genes through MAS.
explore protein dynamics during the differentiation of rice
Prospects for future research: In order to design rice
etioplasts into chloroplasts has led to identification of
genotypes with higher yield and greater stability under low
abundant proteins like chaperones, proteins for
light stress, a better understanding of the anatomical,
photosynthetic energy metabolism, and enzymes of the
physiological, biochemical and molecular basis of low light
tetrapyrrole pathway in etioplasts (Kleffmann et al., 2007).
tolerance is needed. The best approach to overcome this kind
This study also suggests that in the dark, the etioplast
of quantitative problem is to breed new cultivars with high
allocates the main proportion of total protein to carbohydrate
tolerance to low light intensity. Genetic diversity is the
and amino acid metabolism and to regulate the expression
foundation for crop improvement; the traditional varieties
of plastid genes. By using a rice NSF45K oligo-microarray
or landraces of rice harbour a large store of valuable genes
on 2-week-old light and dark grown rice leaf tissue, a set of
that can be used to develop new varieties with improved
365 genes showing significant (8-fold or greater) induction
yield potential (Shanker, 2014). Allele mining is one of the
in light relative to dark conditions has been identified (Jung
promising ways to dissect naturally occurring allelic variants
et al. 2008). A set of rice T-DNA insertional mutants for
of candidate genes with essential agronomic qualities
light-induced genes have been identified and phenotypically
(Ashkani et al., 2015). Edzesi et al. (2016) detected 2953
characterized (Jung et al. 2008). Analysis of a yellow-green
alleles with an average of 11.3 alleles per locus for rice grain
leaf mutant has led identification of a novel rice gene (YGL9)
trait. The increased recombination in MAGIC (Multi-parent
(Wang et al. 2016). This gene is predicted to encode a rice
Advanced Generation Inter Cross) populations can lead to
cpSRP43 protein and comprises a chloroplast transit peptide,
novel rearrangements of alleles and greater genotypic
three chromodomains, and four ankyrin repeats. The
diversity and can be used to generate a gene pool enriched
expression pattern analysis indicated that YGL9 is mainly
in essential traits (Leung et al., 2015). The genes/alleles
expressed in green leaf sheaths and leaves. The quantitative
identified could lead to a set of candidate genes and
real-time PCR analysis also suggests that YGL9 is possibly
development of molecular markers that could make
involved in pigment metabolism, chloroplast development
improvement feasible by marker-assisted selection breeding.
and photosynthesis in rice. Several QTLs have been reported
in rice and role of these QTLs in low light intensity is just Association mapping is increasingly being adopted
being understood. One of the previously reported QTL, as the mapping method of choice. Association mapping
qTSN4 (SPIKE gene) was analyzed with respect to its effect involves searching for genotype-phenotype correlations in
on both C source (flag leaf size, leaf physiology) and sink unrelated individuals (Myles et al., 2009). A total of 126
(panicle size, spikelet number per panicle) (Fabre et al., and 172 significant loci explaining an average of 34.45%
2016). This study concluded that qTSN4 is a promising locus and 39.09% of the phenotypic variation in two environments,
for further physiological studies, particularly under limited respectively, have been identified by association mapping
radiation. In a parallel study, using near-isogenic lines (NILs) for 12 agronomic traits in indica rice (Lu et al., 2015).
in IR64 or IRRI146 background, carrying the QTL qTSN4, Fine-mapping in the post-GWAS era could be a
it was found that under limited light availability qTSN4 effect great strategy for crop improvement for low light stress. A
on panicle spikelet number is indirect, and is induced by fine mapping of qPH6, a novel major quantitative trait locus
assimilate resources at tiller level (Adriani et al., 2016). for plant height in rice carried out using total of 1,791
The proper knowledge in molecular basis of low individuals has delimited to a ~41-kb region containing three
light tolerance will lead to identify candidate genes and annotated genes according to sequence annotation databases.
develop molecular markers that could feasibly be used to The discovery of genes underlying qPH6 might be useful
improve yield by marker assisted selection breeding in a wide for the design and breeding of crops with high grain yield
range of popular rice varieties. Rice the first model crop and quality (Yuan et al., 2015).
plant with publically available high quality genome sequence. Through in sillico analyses, using the various rice,
Since 2004, rice genome sequence has been revolutionized and bioinformatics databases, one can identify the rice genes
our understanding of rice evolution and its synteny with other reported to have a direct or indirect association with different
cereal crops. Decoding of the rice genome sequence also traits under low light conditions. Some of the useful rice
helps for mining DNA based markers to facilitate marker databases are Gramene ([Link]
assisted breeding (Singh et al., 2010). Availability of Oryzabase ([Link] and TIGR
 Volume 38 Issue 3, 2017 213

Fig-1: Number of genes reported in Oryzabase database with different trait class in rice.

Rice Genome Annotation ([Link] association studies to narrow down the candidate genes
these can be used to search genomic regions in rice genome, playing a role in low light intensity tolerance in rice.
developing markers for mapping etc. In the Oryzabase ACKNOWLEDGEMENT
database numbers of genes are reported for different trait This work was supported by DST to SSD and
class of rice (Fig. 1). These genes can then be systematically funding from CAU (Central Agricultural University,
studied through a series of expression analysis and Imphal).
REFERENCES
Adhya, T.K., Singh, O.N. and Ghosh, A. (2008) Rice in Eastern India: Causes for Low Productivity and Available Options. Journal of
Rice Research, 2(1).
Adriani, D.E., Dingkuhn, M., Dardou, A., Adam, H., Luquet, D. and Lafarge, T. (2016). Rice panicle plasticity in near isogenic lines
carrying a QTL for larger panicle is genotype and environment dependent. Rice, 9:28, DOI 10.1186/s12284-016-0101-x.
Ashkani, S., Yusop, M.R., Shabanimofrad, M., Azady, A., Ghasemzadeh, A., Azizi, P. and Latif, M.A. (2015). allele mining strategies:
principles and utilisation for blast resistance genes in rice (Oryza sativa L.). Curr Issues Mol Biol., 17:57-73.
Baloch, J.U.D., Munir, M., Iqbal, M. and Abid, M. (2012). Effects of varied irradiance on flowering time of facultative long day
ornamental annuals. Pakistan Journal of Botany, 44:111-117.
Bang, C.P. and Huyen, T.T.T. (2015). In Silico identification, classification and expression analysis of Genes encoding putative light-
harvesting chlorophyll A/B-binding proteins in Coffee (Coffea Canephora L.). Journal of Agricultural Technology, 11:
2547-2561.
Barmudoi, B. and Bharali, B. (2016). Effects of light intensity and quality on physiological changes in winter rice (Oryza Sativa L.).
International Journal of Environmental & Agriculture Research, 2: 65-76.
Beneragama, C.K. and Goto, K. (2010). Chlorophyll a: b ratio increases under low-light in ‘Shade-tolerant’ Euglena gracilis. Tropical
Agricultural Research, 22: 12 - 25.
214 AGRICULTURAL REVIEWS
Covshoff, S., Furbank, R.T., Leegood, R.C. and Hibberd, J.M. (2013). Leaf rolling allows quantification of mRNA abundance in
mesophyll cells of sorghum. Journal of Experimental Botany, 64:807–813.
Edzesi, W. M., Dang, X., Liang, L., Liu, E., Zaid, I.U. and Hong, D. (2016). Genetic diversity and elite allele mining for grain traits in
rice (Oryza sativa L.) by association mapping. Front. Plant Sci.,| [Link]
Emmanuel, G.A. and Mary, D.M. (2014). Effect of light intensity on growth and yield of a Nigerian local rice variety-Ofada. International
Journal of Plant Research, 4: 89-94.
Fabre, D., Adriani, D.E., Dingkuhn, M., Ishimaru, T., Punzalan, B., Lafarge, T., Clément-Vidal, A. and Luquet, D. (2016). The qTSN4
effect on flag leaf size, photosynthesis and panicle size, benefits to plant grain production in rice, depending on light availability.
Front Plant Sci., 7(623), DOI: 10.3389/fpls.2016.00623.
Fageria, N.K. (2013). Mineral nutrition of rice. CRC press, Taylor and Francis Group. Boca Raton.
Hebbara, M., Rajakumar, G.R., Ravishankar, G. and Raghavaiah, C.V. (2003). Effect of salinity stress on seed yield through physiological
parameters in sunflower genotypes. HELIA, 26:155-160.
Jiao, Y., Ma, L., Strickland, E. and Denga, X.W. (2005). Conservation and divergence of light-regulated genome expression patterns
during seedling development in rice and Arabidopsis. The Plant Cell, 17:3239–3256.
Jiao, D. M. and Li, X. (2001). Cultivar differences in photosynthetic tolerance to photooxidation and shading in rice (Oryza sativa L.).
Photosynthetica, 39: 167–175.
Jung, K.H., Lee, J., Dardick, C., Seo, Y.S., Cao, P., Canlas, P., Phetsom, P., Xu, X., Ouyang, S., An, K., Cho, Yun-Ja., Lee, G.C., Lee,
Y., An, G. and Ronald, P.C. (2008). Identification and functional analysis of light-responsive unique genes and gene family
members in rice. PLoS Genetics, 4:e1000164.
Kleffmann, T., Zychlinski, A., Russenberger, D., Hirsch-Hoffmann, M., Gehrig, P., Gruissem, W. and Baginsky, S. (2007). Proteome
dynamics during plastid differentiation in rice. Plant Physiology, 143:912–923.
Leung, H., Raghavan, C., Zhou, B., Oliva, R., Choi, IR., Lacorte, V., Jubay, M. L.., Cruz, C. V., et al. (2015). Allele mining and
enhanced genetic recombination for rice breeding. Rice (N Y). 2015 Dec; 8:34.
Li, T., Ohsugi, R., Yamagishi, T. and Sasaki, H. (2005). Effects of weak light on rice starch accumulation and starch synthesis enzyme
activities at grain filling stage. Chin. J. Rice Sci., 19: 545–550.
Liu, Q. H., Li, T., Cai, J. and Zhang, J.J. (2006). Effects of shading at different growth stages on amylose and protein contents in rice
grain. Chin. Agric. Sci. Bull., 22: 234–237.
Liu, Q. H., Zhou, X.B., Yang, L.Q., Li, T. and Zhang, J.J. (2009). Effects of early growth stage shading on rice flag leaf physiological
characters and grain growth at grain-filling stage. Chin. J. Appl. Ecol., 20: 2135–2141.
Liu, L., Wang, L., Deng, F., Huang, Y., Liu, D.Y., Ren, W.J. and Yang, W.Y. (2012). Osmotic regulation substance contents and
activities of protective enzymes in leaves of different hybrid rice combinations as affected by shading. Chin J Rice Sci.,
26: 569–575.
Liu, Q.H., Wu, X., Chen, B.C., Ma, J.Q. and Gao, J. (2014). Effects of Low Light on Agronomic and Physiological Characteristics of
Rice Including Grain Yield and Quality. Rice Science, 21: 243"251.
Lu, Q., Zhang, M., Niu, X. et al., (2015). Genetic variation and association mapping for 12 agronomic traits in Indica rice. BMC
Genomics, 16:1067.
Meng, L., Chen, W. F., Li, L. X., Xu, Z. J., Liu, L. X. and Sun, J. W. (2002). Influence of low light on stomatal characters in rice leaves.
J Shenyang Agric Univ., 33: 87–89.
Murchie, E.H. and Horton, P. (1998). Contrasting patterns of photosynthetic acclimation to the light environment are dependent on the
differential expression of the responses to altered irradiance and spectral quality. Plant, Cell and Environment, 21:139–148.
Murchie, E.H., Hubbart, S., Chen, Y.Z., Peng, S.B. and Horton, P. (2002). Acclimation of rice photosynthesis to irradiance under field
conditions. Plant Physiology, 130:1999–2010.
Murchie, E.H., Hubbart, S., Chen, Y.Z., Peng, S.B. and Horton, P. (2005). Acclimation of photosynthesis to high irradiance in rice:
gene expression and interactions with leaf development. Journal of Experimental Botany, 56:449.
Myles, S., Peiffer, J., Brown, P.J., Ersoz, E.S., Zhang, Z., Costich, D.E. and Buckler, E.S. (2009). Association mapping: critical
considerations shift from genotyping to experimental design. The Plant Cell, 21:2194–2202.
Poolman, M.G., Kundu,S., Shaw, R. and Fell, D.A. (2013). Responses to light intensity in a genome-scale model of rice metabolism.
Plant Physiology, 162:1060–1072.
Ren, W.J., Yang, W.Y., Xu, J.W., Fan, G.Q., Wang, L.Y. and Guan, H. (2002). Impact of low-light stress on leaves characteristics of rice
after heading. J Sichuan Agric Univ., 20(3): 205–208.
Restrepo, H. and Garcés, G. (2013). Evaluation of low light intensity at three phenological stages in the agronomic and physiological
responses of two rice (Oryza sativa L.) cultivars. Agronomía Colombiana, 31: 195-200.
Singh, S. (2005). Effect of low-light stress at various growth phases on yield and yield components of two rice cultivars. IRRN, 30: 36-37.
Shanker, A.K. (2014). Physiological and biochemical basis of low light tolerance of selected annual food grain crops with special
relevance to Agroforestry: A transcriptomics approach. [Link]
tolerance/. Accessed 31 August 2016.
Singh, H., Deshmukh, R.K., Singh, A., Singh, A.K., Gaikwad, K., Sharma, T.R., Mohapatra, T. and Singh, N.K. (2010). Highly
variable SSR markers suitable for rice genotyping using agarose gels. Mol. Breed., 25:359–364.
Sridevi, V. and Chellamuthu, V.M. (2015). Impact of weather on rice – A review. International Journal of Applied Research, 1: 825-831.
 Volume 38 Issue 3, 2017 215
Taiz, L. and Zeiger, E. (2010). Plant Physiology (5th ed.). Sinauer Associates, Sunderland, USA.
Tian, L.I., Ohsugi, R., Yamagishi, T. and Sasaki, H. (2006). Effects of Weak Light on Starch Accumulation and Starch Synthesis
Enzyme Activities in Rice at the Grain Filling Stage. Rice Science, 13: 51ÿ58.
Thomas, B. and Vince-Prue, D. (1997). Photoperiodism in Plants. Academic Press, London.
Umate, P. (2010). Genome-wide analysis of the family of light-harvesting chlorophyll a/b-binding proteins in arabidopsis and rice.
Plant Signaling Behavior, 5:12, 1537-1542.
Valladares, F. and Niinemets, U. (2008). Shade Tolerance, a Key Plant Feature of Complex Nature and Consequences. Annual Review
of Ecology, Evolution, and Systematics. 39:237–57.
Venkateswarlu, B. and Visperas, R.M. (1987). Solar radiation and rice productivity. IRRI research paper series 129. International Rice
Research Institute, Manila.
Wang, Z. (2011). Plant Physiology. Beijing: Chinese Agriculture Press: 130–131.
Wang, Z., Zhang, T., Xing, Y., Zeng, X., Wang, L., Liu, Z., Shi, J., Zhu, X., Ma, L., Li, Y., Ling, Y., Sang, X. and He, G. (2016). YGL9,
encoding the putative chloroplast signal recognition particle43 kDa protein in rice, is involved in chloroplast development.
Journal of Integrative Agriculture, 15: 60345-7.
Xiu, D.Y., Xin, J., Jing, Z., Jun-Zhou, L., Hong-Zheng, S. and Quan-Zhi, Z. (2013). Research progress on the impacts of low light
intensity on rice growth and development. Chinese Journal of Eco-Agriculture, 21:1307-1317.
Yamamoto, Y., Kurokawa, H., Nitta, Y. and Yoshida, T. (1995). Varietal differences of tillering response to shading and nitrogen levels
in rice plant: comparison between high tillering semidwaft Indica and low tillering Japonica. Jpn J Crop Sci., 64: 227–234.
Yamori, W., Makino, A. and Shikanai, T. (2016). A physiological role of cyclic electron transport around photosystem I in sustaining
photosynthesis under fluctuating light in rice. Scientific Reports, 6:20147, doi: 10.1038/srep20147.
Yamazaki, J.Y., Kamimura, Y., Okada, M. and Sugimara, Y. (1999). Changes in photosynthetic characteristics and photosystem
stoichiometries in the lower leaves in rice seedlings. Plant Science, 148:155–163.
Yang, D., Duan, L.S., Xie, H.A., Li, Z.H. and Huang, T.X. (2011). Effect of pre-flowering light deficiency on biomass accumulation
and physiological characteristics of rice. Chin J Eco-Agric., 19: 347–352.
Yuan, Y., Miao, J., Tao, Y. (2016). Identification and fine mapping of qPH6, a novel major quantitative trait locus for plant height in
rice. Mol Breeding, 35: 56.
Zervoudakis, G., Salahas, G., Kaspiris, G. and Konstantopoulou, E. (2012). Influence of light intensity on growth and physiological
characteristics of common sage (Salvia officinalis L.). Brazilian archives of biology and technology, 55: 89-95.
Zhu, P., Yang, S.M., Ma, J., Li, S.X. and Chen, Y. (2008). Effect of shading on the photosynthetic characteristics and yield at later
growth stage of hybrid rice combination. Acta Agron Sin., 34: 2003–2009.