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Genetic and Biochemical Mechanisms of Pollen Wall Development

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Genetic and Biochemical Mechanisms of Pollen Wall Development Review Genetic and Biochemical Mechanisms of Pollen Wall Development 1 1 1 1,2 Jianxin Shi, Meihua Cui, Li Yang, Yu-Jin Kim, and 1,3, Dabing Zhang * The pollen wall is a specialized extracellular cell wall matrix that surrounds male Trends gametophytes and plays an essential role in plant reproduction. Uncovering the Pollen wall development exhibits con- fi mechanisms that control the synthesis and polymerization of the precursors of served and diversi ed features. pollen wall components has been a major research focus in plant biology. We Genes associated with pollen wall devel- review current knowledge on the genetic and biochemical mechanisms under- opment are coordinately regulated. lying pollen wall development in eudicot model Arabidopsis thaliana and mono- The synthesis of exine and anther cutin cot model rice (Oryza sativa), focusing on the genes involved in the biosynthesis, may share common pathways in rice. transport, and assembly of various precursors of pollen wall components. The conserved and divergent aspects of the genes involved as well as their regula- tion are addressed. Current challenges and future perspectives are also highlighted. Pollen Wall Development The pollen wall is the complex multiple-layer outer surface of pollen. It is essential for plant reproduction because of its role in rendering male gametophytes resistant to various biotic and abiotic stresses, as well as its function in male–female interaction, fertilization, and seed production [1]. The underlying genetic, molecular, and biochemical mechanisms of pollen wall development have long defied unraveling, but this is changing fast. Several excellent reviews have summarized the genes and enzymes associated with the biosynthesis and transport of the lipidic and phenolic precursors necessary for the formation of the outer pollen wall named exine 1 Joint International Research – [1 4] (see Glossary). In the following we address the evolutionary aspects of the pollen wall Laboratory of Metabolic and Developmental Sciences, Shanghai developmental genes and enzymes from Arabidopsis and rice. The syntheses of pollen exine Jiao Tong University (SJTU)–University and anther cutin appear to share common pathways in the monocot rice, but not in the eudicot of Adelaide Joint Centre for Arabidopsis. In addition, we highlight recent advances in understanding the coordinated Agriculture and Health, State Key Laboratory of Hybrid Rice, School of transcriptional and post-transcriptional regulation of genes involved in pollen wall development. Life Sciences and Biotechnology, Shanghai Jiao Tong University, 800 Based on morphological observations, it has been assumed that the synthesis of pollen wall Dongchuan Road, Shanghai 200240, China starts from meiosis when the callose surrounding the microspore is degraded by callases 2 Department of Oriental Medicinal secreted from the tapetum, a nutritive somatic tissue enclosing microspores. When pro- Biotechnology and Graduate School grammed cell death (PCD)-induced degeneration of tapetal cells takes place during meiosis, of Biotechnology, College of Life Science, Kyung Hee University, young microspores form primexine, a microfibrillar matrix mainly consisting of cellulose that Youngin, 446-701, South Korea acts as an elaborate template for the deposition and assembly of sporopollenin precursors 3 School of Agriculture, Food, and – [1,3 5]. At the stage of pollen maturation, although different plant species display a variety of Wine, University of Adelaide, South Australia 5064, Australia pollen surface morphologies, the mature pollen grains generally contain three layers: the outer exine, the inner intine, and the tryphine (Figure 1) [3,6]. The exine contains three layers from the fl outermost side to the inner side: the reticulate layer, the sexine (baculum and tectum), and a at *Correspondence: fi layer termed the nexine or foot layer. The sexine is usually sculpted in a taxon-speci c manner, [email protected] (D. Zhang). Trends in Plant Science, November 2015, Vol. 20, No. 11 http://dx.doi.org/10.1016/j.tplants.2015.07.010 741 © 2015 Elsevier Ltd. All rights reserved. Uninucleate Premeiosis Tetrad Bicellular pollen Tricellular pollen Glossary microspore Stage ABC subfamily G (ABCG) SP Te Te Ty transporters: the white–brown CW Ty Ba complex (WBC) subfamily of ATP- PE Ba Pb Ne binding cassette (ABC) membrane- PM Ne In transport proteins that facilitate the Arabidopsis In transport of specific substrates SP Te Te across the membrane in an ATP- CW Ty dependent manner. They are half-size PE Ba Ty Ba Rice PM Pb Ne ABC proteins and form hetero- or In In Ne homodimers that function as active Callose wall and Sporopollenin biosynthesis, allocaon, and Inne Tryphine membrane transporters. primexine formaon assembly formaon formaon Key: Anther cuticle: the cuticular lipidic A6 ARF17 AMS/TDR ACOS5 ABCG1 AtUSP CER1 Ba: Baculum AtGSL1 DEX1 AtMYB103 AtACBP4,5,6 ABCG9 CAP1 CER2-LIKES layer that covers the anther surface CW: Callose wall AtGSL5 EFD GAMYB AtAPY6,7 ABCG16 FLA3 FLP1 and protects anthers from biotic and AtTTP NEF1 MS1/PTC1 AtbZIP34 ABCG26 MADS3 LACS1,4 In: Inne Cal5 NPU MYB99 CYP703A2/ ABCG31 OsGT1 PSP1 abiotic stresses. It is composed CDKG1 ROCK1 OsC6 CYP703A3 AtMGT4 Ne: Nexine predominantly of a polymer matrix CDM1 RPG1 TEK CYP704B1/ GLOX1 Pb: Probacula DYT1/UDT1 RPG2 CYP704B2 LTPGs cutin consisting mainly of C16 and Genes GSL5 MS2/DPW OsABCG15 PE: Primexine C18-hydroxy fatty acids that is OsG1 OsUAM3 OsC6 PM: Plasma membrane TDF1 PKSA Type III LTPs covered and embedded with distinct PKSB SP: Sporopollenin precursor very-long-chain (C24–C34) saturated RBOHE Te: Tectum TKPR1 and unsaturated non-polar waxes. TKPR2 Ty: Tryphine Cuticle in the surface of plant tissues other than anther is synthesized exclusively by the epidermal cells. By contrast, anther cuticle seems to be Figure 1. Comparison of Genes/Enzymes Involved in Various Stages of Pollen Wall Development in synthesized mainly in the tapetum, Arabidopsis and Rice. Stages from pre-meiosis to tricellular pollen are defined in [2]. The scanning electronic microscopy the innermost layer of the anther wall. (SEM) and transmission electronic microscopy (TEM) images are both from mature pollen (scale bars from top left to bottom Callose: also known as b-glucan, is right are 1, 10, 30, 1, 20, and 1 mm, respectively). Pollen wall development-associated genes/enzymes identified in synthesized at the cell wall by callose Arabidopsis and rice are indicated in black and red, respectively. synthases and degraded by b-1,3- glucanases. This specific cell wall polymer functions in several fundamental biological processes, ranging from plant development to fi and this is one of the important features for species identi cation. The nexine functions as a the response to abiotic and biotic skeleton for exine formation. The biochemical nature of exine has remained largely unknown stresses. During angiosperm microsporogenesis, callose serves as owing to its unusual insolubility and extreme stability. Its major constituent has been found to be a temporary wall to separate newly sporopollenin, a biopolymer mainly consisting of polyhydroxylated aliphatic compounds and formed microspores in the tetrad fi phenolics [7,8]. Although sporopollenin commonly exists in pollens and spores [9], the ne from microsporocytes. The development of pollen wall originates structure of exine and the relative amount of each stratum vary between species. For example, from the callose wall, and the callose insect- or self-pollinated pollen in Arabidopsis has a sculptured surface with reticulate cavities wall around the tetrad may recruit the filled with abundant tryphines, whereas wind-pollinated rice or maize pollen has a smooth primexine and together provide a fi surface with a continuous tectum and cavities between tectum and nexine that are lled with structural support for exine formation. Abnormal callose deposition and much less tryphines [3,6,10,11]. This species-specialized pollen wall patterning has also been an dissolution often leads to male intriguing subject of study for researchers. sterility. Elaioplasts: a type of non- Given the diversity of plant species and the complexity of pollen structures [3], as well as the pigmented and specialized plastid (leucoplast) derived from proplastids limitations of current chemical fixation methods in the preservation of the ultracellular structures for the storage of steryl esters, free of tapetal organelles and pollen wall components [12], it is difficult to draw a single and unified polar lipids, and plastid lipid- developmental timing-scheme of pollen wall development for all plants. We focus on the recent associated proteins in Brassicaceae advances obtained from the dicot Arabidopsis and from monocot rice (Figure 1 and Table S1 in species. Exine: the most complex and the supplemental information online). important outer layer of the pollen wall. Generally contains two layers, Genes Involved in Pollen Wall Development the inner nexine and the outer sexine. Callose Biosynthesis and Degradation The nexine has a bilayer structure, consisting of nexine I and nexine II, Callose is synthesized by callose synthase (CalS). It surrounds the newly formed microspores to and the sexine is further composed act as the mold for primexine, and its degradation by b-1,3-glucanases facilitates the release of of tectum and bacula. The portions microspores from the tetrad. Arabidopsis CalS5 [13], GLUCAN SYNTHASE-LIKE 1 and 12 742 Trends in Plant Science, November 2015, Vol. 20,
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