Journal of Integrative Plant Biology 2013, 55 (7): 572–575
Invited Expert Review
Boosting Seed Development as a New Strategy to Increase Cotton Fiber Yield and Quality Yong‐Ling Ruan1,2* 1
Department of Biology, School of Environmental and Life Sciences, The University of Newcastle, Callaghan, 2308 New South Wales, Australia, Australia‐China Research Centre for Crop Improvement, The University of Newcastle, Callaghan, 2308 New South Wales, Australia Corresponding author E‐mail:
[email protected] Articles can be viewed online without a subscription. Available online on 29 May 2013 at www.jipb.net and www.wileyonlinelibrary.com/journal/jipb doi: 10.1111/jipb.12074 2
Abstract Cotton (Gossypium spp.) is the most important textile crop worldwide due to its cellulosic mature fibers, which are single‐celled hairs initiated from the cotton ovule epidermis at anthesis. Research to improve cotton fiber yield and quality in recent years has been largely focused on identifying genes regulating fiber cell initiation, elongation and cellulose synthesis. However, manipulating some of those candidate genes has yielded no effect or only a marginally positive effect on fiber yield or quality. On the other hand, evolutionary comparison and transgenic studies have clearly shown that cotton Yong‐Ling Ruan (Corresponding author) fiber growth is intimately controlled by seed development. Therefore, I propose that enhancing seed development could be a more effective and achievable strategy to increase fiber yield and quality. Keywords:
Auxin; cotton fiber; seed development; sugars; seed maternal and filial tissues.
Ruan YL (2013) Boosting seed development as a new strategy to increase cotton fiber yield and quality J. Integr. Plant Biol. 55(7), 572–575.
Introduction Cotton (Gossypium spp.) is the most important textile and oil crop worldwide. The cellulose‐enriched mature fibers (lint) develop from the seed coat epidermis as single‐celled hairs, whereas the embryo synthesizes oils and proteins. As such, both the maternal and filial tissues of cotton seed are of major economic significance, which is rare among domesticated plant species. Among the genus Gossypium L., four species are cultivated: the tetraploid species of G. hirsutum and G. barbadense, and two diploids, G. herbaceum and G. arboretum (Brubaker et al. 1999). G. hirsutum is the most cultivated species, accounting for about 90% of the global cotton fiber production. Thus, most of the research on cotton fiber development has been conducted on G. hirsutum (Ruan 2005, and references therein). Hence, this review focuses on studies derived from G. hirsutum, unless otherwise stated.
© 2013 Institute of Botany, Chinese Academy of Sciences
The developmental program of cotton fiber has been intensively studied (see reviews by Basra and Malik 1984; Ruan 2007; Qin and Zhu 2011). In short, these single cells initiate from the ovule epidermis at or just prior to anthesis, and then elongate rapidly for about two to three weeks to a final length of 2.5 to 3.0 cm. At the end of the elongation, fiber cells synthesize a massive amount of cellulose. By maturity, more than 90% of fiber dry weight is cellulose. The fiber cell number, their length and the amount of cellulose deposited in the cell walls collectively determine cotton fiber yield and quality. Not surprisingly, a huge effort has been made over the last two decades to identify the genes regulating various aspects of cotton fiber development with an ultimate goal to improve fiber yield and quality by using biotechnological approaches (e.g. Ruan et al. 2003; Xu et al. 2007). Interestingly, manipulating some of those identified ‘key’ genes in the fibers results in little or only a marginally positive effect on fiber yield or quality. On the
Boosting Seed Development to Increase Fiber Yield
other hand, there is compelling evidence that fiber growth is in fact largely controlled by seed development. This essay provides analyses to support the view that significant improvement in cotton fiber yield and quality could be achieved through the enhancement of cotton seed development. Apart from the predicted positive effect on fiber production, this approach could have an added benefit of increasing seed oil yield.
Manipulating Fiber Genes May Be Insufficient to Exert a Positive Impact on Fiber Yield and Quality The fiber initiation process determines fiber number, and hence yield potential. The process is regulated by complex gene networks and signalling pathways. To this end, an MYB transcription factor, R2R3MYB, GhMYB25‐like, has been identified as a positive regulator of fiber initiation since (i) it was predominately expressed in fiber initials and (ii) silencing its expression resulted in a fiberless seed phenotype, resembling that in the XU142 fiberless mutant (Walford et al. 2011). However, increasing the transcript level of GhMYB25‐like driven by its own promoter did not increase fiber number in the transgenic plants (Walford et al. 2011). Sucrose synthase (Sus) is another key player in fiber initiation and subsequent development. It canalizes the cleavage reaction of sucrose in the presence of UPD into UDP‐glucose and fructose, and plays a major role in metabolic regulation and sugar signalling. Silencing Sus expression led to a fiberless seed phenotype (Ruan et al. 2003). However, similar to the fate of GhMYB25‐like, over‐expression of Sus using a fiber specific promoter failed to produce a visible positive effect on mature fibers (Ruan, unpublished data). The above case studies show that inhibition of fiber cells by silencing the expression of a candidate gene does not necessarily indicate the achievement of a positive effect on the fiber phenotype through its over‐expression in the fibers. This suggests limitations in improving fiber productivity by manipulating fiber genes within fibers.
Fiber Cells are Intimately Regulated by Seed Development An important fact that has been largely ignored in our endeavour to understand cotton fiber biology for increasing fiber yield or quality is that fiber is part of the seed and its development is tightly controlled by seed development. Below are some examples supporting this conclusion from evolutionary and transgenic perspectives. First, an increase in cotton fiber yield has been strongly correlated with an increase in seed size through evolution and domestication (Applequist et al. 2001; Pugh et al. 2010). This
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correlation could be attributed to the corresponding capacity of the seed in mobilizing nutrient resources to the filial tissues (Pugh et al. 2010). Therefore, fiber development in the big seed species or cultivars most likely benefits from the high sink strength of these seeds, leading to the production of longer or more fibers. Second, suppressing embryo or endosperm development by silencing Sus blocked seed—and hence fiber—development entirely, whereas repressing Sus in the seed coat inhibited fiber growth but had no negative effect on seed development (Ruan et al. 2003; Ruan et al. 2008). Consistently, seed development appears to not be affected among all fiberless mutants in the tetraploid cotton species. These data show that fiber development is dependent upon seeds, but not the other way around. More recently, Xu et al. (2012) found that over‐expression of Sus driven by a promoter active in cotton embryo as well as fiber and leaves increased seed number by 22% which translated to an 18% increase in mature fiber weight. The phenotype is due to an increase in seed sink strength, thereby alleviating seed abortion (Xu et al. 2012). This is in contrast to the absence of a positive effect on mature fiber in transgenic cotton, where Sus has been specifically over‐expressed in fibers (see early discussion). This comparison demonstrates that boosting seed development is an effective way to improve fiber development. Third, indole‐3‐acetic acid (IAA) is a well‐known auxin hormone that stimulates fiber initiation and elongation based on in vitro culture studies (Basra and Malik 1984; Kim and Triplett 2001). However, early attempts to increase fiber production through over‐expressing IAA biosynthetic genes using a fiber‐specific promoter did not affect fiber growth, despite a significant increase in the free IAA content in transgenic fibers (John 1999). Recently, Zhang et al. (2011) reported that expression of the IAA biosynthetic gene iaaM, under the control of the promoter for the petunia MADS box gene Floral Binding Protein 7 (FBP7), significantly increased fiber cell number and final yield and quality. While the data were interpreted by Zhang et al. (2011) as a fiber‐cell specific effect, the FBP7 promoter is known to be active in the entire ovule and seed coat (Colombo et al. 1997). Thus, the positive impact on fiber initiation observed in the iaaM over‐expressed cotton may well be due to enhanced IAA biosynthesis within the ovules. Significantly, exogenous application of an IAA transport inhibitor, 1‐naphthylphthalamic acid (NPA), to wild‐type cotton ovary pedicels three d before flowering dramatically reduced IAA content and the number of fiber cells (Zhang et al. 2011). This latter observation strongly indicates that IAA in fiber initials is imported from underlying ovule tissues, rather than synthesized within the fibers. Consistent with the above analyses is the spatially asymmetric distribution of fiber initiation along the ovule epidermis being earlier and greater in the ovule chalaza region than in the micropylar end. It has been suggested that fiber initials at the chalaza end may have an advantage in acquiring essential
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nutrients and signalling molecules such as sugars, and IAA imported from the adjacent phloem terminus (Ruan 2005). Taken together, the above examples show that fiber initiation, and hence yield potential, are controlled more by ovules than by fibers themselves.
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A
Wild type
Fiber Aborted seed Seed
Towards Improving Fiber Production by Boosting Seed Development: Where to Start? Increasing seed number A common phenomenon conserved among all cotton species is that only about 25–30% of ovule epidermal cells develop to fiber cells at anthesis (Applequist et al. 2001). While increasing the proportion of fibers from the ovule epidermis remains an attractive approach to achieving higher fiber yield (Zhang et al. 2011), an increase in seed number will most likely translate into more fiber cells per boll. Indeed, there is a strong correlation between the number of seeds and the production of fibers in both tetraploid and diploid cotton species (Applequist et al. 2001). This goal may be achieved through either an increase in ovule number or a decrease in seed abortion (Figure 1A). Seed and fruit abortion is a major problem in global food and fiber security, as it causes irreversible yield loss (Ruan et al. 2012). In wild‐type cotton, about 20% of developing seeds are aborted under normal growth conditions (Ruan et al. 2003), with more abortion occurring under drought, cold and heat stress. The observation that enhancing Sus expression reduced seed abortion resulting in a significant increase in fiber production (Xu et al. 2012) demonstrates great potential in improving fiber yield through an increase in seed number.
Increasing seed size The number of fibers produced per seed is limited by the surface area of the epidermis. It follows that, the larger the seed, the more the fibers, as was the case in the evolution and domestication of cotton (Applequist et al. 2001). One may argue that an increase in seed size or number may be difficult to achieve, as seeds are physically confined by the surrounding fruit tissue, the pericarp (Figure 1A). However, strong evidence indicates that fruit development, including that in cotton, is controlled by seeds (Ruan et al. 2003). Thus, it can be predicted that enhancing seed size will increase fruit volume accordingly. Seed size is determined by cell division and cell expansion regulated by diverse gene expression and signalling pathways. To this end, glucose and auxin are potent signals to stimulate cell division early in seed development through the activation of cell cycle genes (Ruan et al. 2012). Consistently, high activity of cell wall invertase (CWIN), hydrolysing sucrose into glucose and
Seed boosted
Pericarp
B
f v
f
tc
v tc
e
v
v
e sc
sc
v
Figure 1. Schematic diagram on strategies to increase cotton fiber production by booting seed development. (A) Increase in fiber number by increasing seed number. This may be achieved by increasing ovule number or reducing seed abortion. (B) Increase in fiber production by enhancing seed size. This may be achieved through enhancing the development of embryonic tissue and the transfer cell, and thereby the overall seed sink strength. e, embryo; f, fiber; sc, seed coat, tc, transfer cell; v, vascular bundle.
fructose, correlates with cell division intensity and seed size in faba bean (Weber et al. 1996), maize (Vilhar et al. 2002) and rice (Wang et al. 2010). Seed size is known to be controlled by metabolic interaction between maternal and filial tissues. In this context, seeds from many crop species including cotton develop transfer cells (TCs) at the interface of the maternal seed coat and the endosperm or embryo (Figure 1B). TCs are specialized cells displaying invaginated wall ingrowths (WIs), thereby amplifying their plasma membrane surface area and hence their capacity to transport nutrients (Offler et al. 2003). Cotton seed TCs are located at the innermost layer of the seed coat, and are predicted to play a major role in channelling nutrients to the embryonic tissues (Figure 1B). The degree of WIs of cotton seed TCs, and hence their membrane surface, highly correlates with seed size and fiber yield (Pugh et al. 2010). Development of TCs is under the control of transcriptional and metabolic regulation by a cohort of transcription factors (e.g. Myb‐Related Protein‐1; Gómez et al. 2009) and enzymes such as Sus in cotton seed TCs (Pugh et al. 2010). The above information provides useful avenues to
Boosting Seed Development to Increase Fiber Yield
enhance cotton seed size by manipulating relevant gene targets or cellular processes, thereby increasing fiber production (Figure 1B).
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Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: Cells specialized for a special purpose. Ann. Rev. Plant Biol. 54, 431– 454. Qing YM, Zhou YX (2011) How cotton fibers elongate: A tale of linear cell‐growth mode. Curr. Opin. Plant Biol. 14, 106–111.
Conclusions
Ruan YL (2005) Recent advances in understanding cotton fibre and seed
Cotton fiber development is tightly regulated by overall seed development. Thus, any attempts to increase fiber production should be carried out in the context of seed development rather than solely focusing on fiber itself. The analyses in this essay argue that significant improvement in fiber yield and quality could be achieved by manipulating genes and cellular processes controlling seed number, size and their overall sink strength.
Ruan YL (2007) Insights into the rapid cell expansion and cellulose
development. Seed Sci. Res. 15, 269–280. synthesis mediated by plasmodesmata and sugar: Insights from the single‐celled cotton fibre. Funct. Plant Biol. 34, 1–10. Ruan YL, Llewellyn DJ, Furbank RT (2003) Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation and seed development. Plant Cell 15, 952–964. Ruan YL, Llewellyn DJ, Liu Q, Xu SM, Wu LM, Wang L, Furbank RT (2008) Expression of sucrose synthase in the developing endosperm is essential for early seed development in cotton. Funct. Plant Biol.
Acknowledgements
35, 382–393. Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012)
The work in the author’s laboratory was supported by the Australian Research Council (grant numbers DP110104931 and DP120104148) and the Australian Federal Government, Department of Industry, Innovation, Science, Research and Tertiary Education (Grant number ACSRF00981).
Molecular regulation of seed and fruit set. Trends Plant Sci. 17, 656– 665. Pugh DA, Offler CE, Talbot MJ, Ruan YL (2010) Evidence for the role of transfer cells in the evolutionary increase of seed and fiber biomass yield in Cotton. Mol. Plant 3, 1075–1086. Vilhar B, Kladnik A, Blejec A, Chourey PS, Dermastia M (2002)
Received 7 May 2013
Accepted 15 May 2013
Cytometrical evidence that the loss of seed weight in the miniature1 seed mutant of maize is associated with reduced mitotic activity in the developing endosperm. Plant Physiol. 129, 23–30.
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(Co‐Editor: Yuxian Zhu)
