Special Issue: Plant Reproduction and Fertility   

August 2009, Volume 51 Issue 8, Pages 718-811.

Cover Caption: Plant Reproduction and Fertility
Endocytic pathways meet secretion in pollen tube: positively charged nanogold is internalised in the organelle rich zone (black arrows) by clathrin-dependent (CD) (yellow) and clathrin independent endocytosis (green). In the first case, endocytic vesicles are recycled to exocytosis through the Golgi apparatus (red arrows); in the second case, vesicles are transported to the TGN and then directed to the degradation pathway (black arrows). Negatively charged nanogold is internalised in the clear zone (pink and orange vesicles, blue arrows). Note that internalization of plasma membrane in the tip contributes to the V-shaped vesicles accumulation in the apex. Please go to pages 727-739 for details (cover design: Ying Wang).


Sexual Plant Reproduction: a Fertile and Flourishing Field  
Author: Mengxiang Sun
Journal of Integrative Plant Biology 2009 51(8): 718-718
Published Online: August 2, 2009
DOI: 10.1111/j.1744-7909.2009.00860.x

Since the very beginning of plant science, sexual plant reproduction (SPR) has proved an attractive and enduring topic for generations of botanists. With the rapid development of modern technology, a significant acceleration has occurred in our understanding on the developmental mechanisms of plant reproductive processes, particularly the evolution of double fertilisation, signalling in pollen tube orientation, molecular characterisation of plant gametes, maternal to zygotic transitions and parental gene involvement in early embryogenesis. This is reflected not only by several recent high-ranking research papers, but also by the frequent conferences and workshops on these topics. These include the 2008 XXth International Congress on SPR in Bras´żlia and “Frontiers in SPR III” in Tucson, as well as “Cell-Cell Communication in Plant Reproduction” held in 2009 in Bath. The continuing efforts from around the world indicate that SPR is still a fertile and flourishing field, with great expectations for the coming decade.

Investigations on SPR have been enhanced recently by their underlying relationship to agriculture. With the development of molecular crop breeding comes an increasing requirement for knowledge on molecular mechanisms of SPR, both general regulatory processes, and in particular, signalling for cell-cell communication in several critical steps. To reveal mechanisms behind some well-known phenomena in modern agriculture, such as compatibility of crop crosses and fertility determination of remote hybrids and heterosis, one must first precisely understand the basic developmental processes and molecular mechanisms involved in SPR. Thus, it is not surprising that the field has attracted much attention in recent years. In fact, advances in the study of SPR throw new light on investigations for solving many existing problems in agriculture.

This special issue presents current research on multiple aspects of SPR, both pre- and post-fertilisation. Hence, this special issue of the Journal of Integrative Plant Biology features a diverse collection of papers. One paper, “The earliest normal flower in Liaoning Province, China” (see pages 800–811), presents evidence of component parts and morphology of early angiosperm flowers. Four papers, “A genome-wide functional characterisation of Arabidopsis regulatory calcium sensors in pollen tubes” (see pages 751–761), “GNOM-LIKE 2, encoding an ARF-GEF protein homologous to GNOM and GNL1, is essential for pollen germination in Arabidopsis” (see pages 762–773), “Regulation of actin dynamics in the pollen tubes:control of actin polymer level” (see pages 740–750) and “Pollen tube growth: a delicate equilibrium between secretory and endocytic pathways” (see pages 727–739), deal with molecular mechanisms of pollen tube growth and orientation, a hot field in SPR. Amongst these papers, Prof. Moscatelli offers a deep insight into dynamic control of vesicle trafficking in pollen tubes. In the signalling cascade of vesicle trafficking, calcium and actin dynamics play essential roles in the balance between secretory and endocytic pathways. GNOM-LIKE 2, as an ARF-GEF- and BFA-sensitive protein,may indirectly influence calcium and actin dynamics during pollen germination and pollen tube growth.

“Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice” (see pages 774–781) presents new evidence for the interaction between tapetum and pollen development. “Comparative detection of calcium fluctuations in single female sexual cells of tobacco to distinguish calcium signals triggered by in vitro fertilisation” (see pages 782–791) reports observations on calcium dynamics during sperm-central cell fusion, and “Oil body biogenesis during Brassica napus embryogenesis” (see pages 792–799) focuses on post-fertilisation developmental events, mainly on oil body generation and accumulation during embryogenesis in both wild type and mutants. A review paper, “Analyses of sexual reproductive success in transgenic and/or mutant plants” (see pages 719–726), gives a critical evaluation of current techniques used for investigating genes that affect pistil development, and provides useful information and technical guidance to readers in this field. These papers coherently address the common theme: development and its mechanisms in plant reproductive processes. In this way, we hope to create an atmosphere in which extensive discussion can stimulate and lead to interactions between scientists with different perspectives in order to inspire future directions.

We sincerely hope that this special issue of JIPB will provide a platform to highlight current advances and novel findings in the study of SPR. Finally, we express our appreciation to JIPB for supporting this special issue and to all authors for their great contributions. Mengxiang Sun, Professor The Editor for this Special Issue College of Life Sciences, Wuhan University, China

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          Invited Expert Reviews
Analyses of Sexual Reproductive Success in Transgenic and/or Mutant Plants  
Author: Cristiane P. G. Calixto, Gustavo H. Goldman and Maria Helena S. Goldman
Journal of Integrative Plant Biology 2009 51(8): 719-726
Published Online: July 7, 2009
DOI: 10.1111/j.1744-7909.2009.00845.x

The pistil, the female reproductive organ of plants, is a key player in the success of sexual plant reproduction. Ultimately, the production of fruits and seeds depends on the proper pistil development and function. Therefore, the identification and characterization of pistil expressed genes is essential for a better understanding and manipulation of the plant reproduction process. For studying the function of pistil expressed genes, transgenic and/or mutant plants for the genes of interest are used. The present article provides a review of methods already exploited to analyze sexual reproductive success. It intends to supply useful information and to guide future experiments in the study of genes affecting the pistil development and function.

Calixto CPG, Goldman GH, Goldman MHS (2009). Analyses of sexual reproductive success in transgenic and/or mutant plants. J. Integr. Plant Biol. 51(8), 719-726.

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Pollen Tube Growth: a Delicate Equilibrium Between Secretory and Endocytic Pathways  
Author: Alessandra Moscatelli and Aurora Irene Idilli
Journal of Integrative Plant Biology 2009 51(8): 727-739
Published Online: August 2, 2009
DOI: 10.1111/j.1744-7909.2009.00842.x

Although pollen tube growth is a prerequisite for higher plant fertilization and seed production, the processes leading to pollen tube emission and elongation are crucial for understanding the basic mechanisms of tip growth. It was generally accepted that pollen tube elongation occurs by accumulation and fusion of Golgi-derived secretory vesicles (SVs) in the apical region, or clear zone, where they were thought to fuse with a restricted area of the apical plasma membrane (PM), defining the apical growth domain. Fusion of SVs at the tip reverses outside cell wall material and provides new segments of PM. However, electron microscopy studies have clearly shown that the PM incorporated at the tip greatly exceeds elongation and a mechanism of PM retrieval was already postulated in the mid-nineteenth century. Recent studies on endocytosis during pollen tube growth showed that different endocytic pathways occurred in distinct zones of the tube, including the apex, and led to a new hypothesis to explain vesicle accumulation at the tip; namely, that endocytic vesicles contribute substantially to V-shaped vesicle accumulation in addition to SVs and that exocytosis does not involve the entire apical domain. New insights suggested the intriguing hypothesis that modulation between exo- and endocytosis in the apex contributes to maintain PM polarity in terms of lipid/protein composition and showed distinct degradation pathways that could have different functions in the physiology of the cell. Pollen tube growth in vivo is closely regulated by interaction with style molecules. The study of endocytosis and membrane recycling in pollen tubes opens new perspectives to studying pollen tube-style interactions in vivo.

Moscatelli A, Idilli AI (2009). Pollen tube growth: a delicate equilibrium between secretory and endocytic pathways. J. Integr. Plant Biol. 51(8), 727–739.

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Regulation of Actin Dynamics in Pollen Tubes: Control of Actin Polymer Level  
Author: Naizhi Chen, Xiaolu Qu, Youjun Wu and Shanjin Huang
Journal of Integrative Plant Biology 2009 51(8): 740-750
Published Online: June 24, 2009
DOI: 10.1111/j.1744-7909.2009.00850.x

Actin cytoskeleton undergoes rapid reorganization in response to internal and external cues. How the dynamics of actin cytoskeleton are regulated, and how its dynamics relate to its function are fundamental questions in plant cell biology. The pollen tube is a well characterized actin-based cell morphogenesis in plants. One of the striking features of actin cytoskeleton characterized in the pollen tube is its surprisingly low level of actin polymer. This special phenomenon might relate to the function of actin cytoskeleton in pollen tubes. Understanding themolecularmechanism underlying this special phenomenon requires careful analysis of actin-binding proteins that modulate actin dynamics directly. Recent biochemical and biophysical analyses of several highly conserved plant actin-binding proteins reveal unusual and unexpected properties, which emphasizes the importance of carefully analyzing their action mechanism and cellular activity. In this review, we highlight an actin monomer sequestering protein, a barbed end capping protein and an F-actin severing and dynamizing protein in plant. We propose that these proteins function in harmony to regulate actin dynamics and maintain the low level of actin polymer in pollen tubes.

Chen N, Qu X, Wu Y, Huang S (2009). Regulation of actin dynamics in pollen tubes: control of actin polymer level. J. Integr. Plant Biol. 51(8), 740–750.

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          Research Articles
A Genome-wide Functional Characterization of Arabidopsis Regulatory Calcium Sensors in Pollen Tubes  
Author: Liming Zhou, Ying Fu and Zhenbiao Yang
Journal of Integrative Plant Biology 2009 51(8): 751-761
Published Online: June 24, 2009
DOI: 10.1111/j.1744-7909.2009.00847.x

Calcium, an ubiquitous second messenger, plays an essential and versatile role in cellular signaling. The diverse function of calcium signals is achieved by an excess of calcium sensors. Plants possess large numbers of calcium sensors, most of which have not been functionally characterized. To identify physiologically relevant calcium sensors in a specific cell type, we conducted a genome-wide functional survey in pollen tubes, for which spatiotemporal calcium signals are well-characterized and required for polarized tip growth. Pollen-specific members of calmodulin (CaM), CaM-like (CML), calcium-dependent protein kinase (CDPK) and calcineurin B-like protein (CBL) families were tagged with green fluorescence protein (GFP) and their localization patterns and overexpression phenotypes were characterized in tobacco pollen tubes. We found that several fusion proteins showed distinct overexpression phenotypes and subcellular localization patterns. CDPK24-GFP was localized to the vegetative nucleus and the generative cell/sperms. CDPK32-GFP caused severe growth depolarization. CBL2-GFP and CBL3-GFP exhibited dynamic patterns of subcellular localization, including several endomembrane compartments, the apical plasma membrane (PM), and cytoskeleton-like structures in pollen tubes. Their overexpression also inhibited pollen tube elongation and induced growth depolarization. These putative calcium sensors are excellent candidates for the calcium sensors responsible for the regulation of calcium homeostasis and calciumdependent tip growth and growth oscillation in pollen tubes.

Zhou L, Fu Y, Yang Z (2009). A genome-wide functional characterization of Arabidopsis regulatory calcium sensors in pollen tubes. J. Integr. Plant Biol. 51(8), 751–761.

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GNOM-LIKE 2, Encoding an Adenosine Diphosphate-Ribosylation Factor Guanine Nucleotide Exchange Factor Protein Homologous to GNOM and GNL1, is Essential for Pollen Germination in Arabidopsis  
Author: Dong-Jie Jia, Xi Cao, Wei Wang, Xiao-Yun Tan, Xue-Qin Zhang, Li-Qun Chen and De Ye
Journal of Integrative Plant Biology 2009 51(8): 762-773
Published Online: August 2, 2009
DOI: 10.1111/j.1744-7909.2009.00858.x

In flowering plants, male gametes are delivered to female gametophytes by pollen tubes. Although it is important for sexual plant reproduction, little is known about the genetic mechanism that controls pollen germination and pollen tube growth. Here we report the identification and characterization of two novel mutants, gnom-like 2-1 (gnl2-1) and gnl2-2 in Arabidopsis thaliana, in which the pollen grains failed to germinate in vitro and in vivo. GNL2 encodes a protein homologous to the adenosine diphosphate-ribosylation factor-guanine nucleotide exchange factors, GNOM and GNL1 that are involved in endosomal recycling and endoplasmic reticulum-Golgi vesicular trafficking. It was prolifically expressed in pollen grains and pollen tubes. The results of the present study suggest that GNL2 plays an important role in pollen germination.

Jia DJ, Cao X, Wang W, Tan XY, Zhang XQ, Chen LQ, Ye D (2009). GNOM-LIKE 2, encoding anadenosine diphosphate-ribosylation factor- guanine nucleotide exchange factor protein homologous to GNOM and GNL1, is essential for pollen germination in Arabidopsis. J. Integr. Plant Biol. 51(8), 762–773.

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Premature Tapetum Degeneration: a Major Cause of Abortive Pollen Development in Photoperiod Sensitive Genic Male Sterility in Rice  
Author: Yinlian Shi, Sha Zhao and Jialing Yao
Journal of Integrative Plant Biology 2009 51(8): 774-781
Published Online: July 3, 2009
DOI: 10.1111/j.1744-7909.2009.00849.x

Photoperiod-sensitive genic male-sterile (PSGMS) rice (Oryza sativa L.), a natural mutant found in the rice cultivar Nongken 58, is very useful for the development of hybrid rice cultivars. Despite its widespread use in breeding programs, the initial stage of the abortive development of PSGMS rice and the possible cytological mechanisms of pollen abortion have not been determined. In the present study, a systematic cytological comparison of the anther development of PSGMS rice with its normal fertile counterpart is conducted. The results show that pollen abortion in PSGMS rice first occurs before the pollen mother cell (PMC) stage, and continues during the entire process of pollen development until pollen degradation. The abortive process was closely associated with the abnormal behavior of the tapetum. Although tapetum degeneration in PSGMS rice initiates already at the PMC stage, it proceeds slowly and does not complete until the breakdown of the pollen. Such cytological observations were supported by the results of the TUNEL (TdT mediated dUTP Nick End Labeling) assay, which detects DNA fragmentation resulting from programmed cell death (PCD), indicating that the premature tapetum degeneration is in the process of PCD.

Shi Y, Zhao S, Yao J (2009). Premature tapetum degeneration: a major cause of abortive pollen development in photoperiod sensitive genic male sterility in rice. J. Integr. Plant Biol. 51(8), 774-781

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Comparative Detection of Calcium Fluctuations in Single Female Sexual Cells of Tobacco to Distinguish Calcium Signals Triggered by in Vitro Fertilization  
Author: Xiong-Bo Peng, Mengxiang Sun and Hongyuan Yang
Journal of Integrative Plant Biology 2009 51(8): 782-791
Published Online: August 2, 2009
DOI: 10.1111/j.1744-7909.2009.00857.x

Double fertilization is a key process of sexual reproduction in higher plants. The role of calcium in the activation of female sex cells through fertilization has recently received a great deal of attention. The establishment of a Ca2+-imaging technique for living, single, female sex cells is a difficult but necessary prerequisite for evaluating the role of Ca2+ in the transduction of external stimuli, including the fusion with the sperm cell, to internal cellular processes. The present study describes the use of Fluo-3 for reporting the Ca2+ signal in isolated, single, female sex cells, egg cells and central cells, of tobacco plants. A suitable loading protocol was optimized by loading the cells at pH 5.6 with 2 μM Fluo-3 for 30 min at 30◦C. Under these conditions, several key factors related to in vitro fertilization were also investigated in order to test their possible effects on the [Ca2+]cyt of the female sex cells. The results indicated that the bovine serum albumin-fusion system was superior to the polyethlene glycol-fusion system for detecting calcium fluctuations in female sex cells during fertilization. The central cell was fertilized with the sperm cell in bovine serum albumin; however, no evident calcium dynamic was detected, implying that a transient calcium rise might be a specific signal for egg cell fertilization.

Peng X-B, Sun M-X, Yang H-Y (2009). Comparative detection of calcium fluctuations in single female sex cells of tobacco to distinguish calcium signals triggered by in vitro fertilization. J. Integr. Plant Biol. 51(8), 782–791.

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Oil Body Biogenesis during Brassica napus Embryogenesis  
Author: Yu-Qing He and Yan Wu
Journal of Integrative Plant Biology 2009 51(8): 792-799
Published Online: June 24, 2009
DOI: 10.1111/j.1744-7909.2009.00851.x

Although the oil body is known to be an important membrane enclosed compartment for oil storage in seeds, we have little understanding about its biogenesis during embryogenesis. In the present study we investigated the oil body emergence and variations in Brassica napus cv. Topas. The results demonstrate that the oil bodies could be detected already at the heart stage, at the same time as the embryos began to turn green, and the starch grains accumulated in the chloroplast stroma. In comparison, we have studied the development of oil bodies between Arabidopsis thaliana wild type (Col) and the low-seed-oil mutant wrinkled1–3. We observed that the oil body development in the embryos of Col is similar to that of B. napus cv. Topas, and that the size of the oil bodies was obviously smaller in the embryos of wrinkled1–3. Our results suggest that the oil body biogenesis might be coupled with the embryo chloroplast.

He YQ, Wu Y (2009). Oil body biogenesis during Brassica napus embryogenesis. J. Integr. Plant Biol. 51(8), 792–799.

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The Earliest Normal Flower from Liaoning Province, China  
Author: Xin Wang and Shaolin Zheng
Journal of Integrative Plant Biology 2009 51(8): 800-811
Published Online: June 4, 2009
DOI: 10.1111/j.1744-7909.2009.00838.x

The early evolution of angiosperms has been a focus of intensive research for more than a century. The Yixian Formation in western Liaoning yields one of the earliest angiosperm macrofloras. Despite multitudes of angiosperm fossils uncovered, including Archaefructus and Sinocarpus, no bona fide normal flower has been dated to 125 Ma (mega-annum) or older. Here we report Callianthus dilae gen. et sp. nov. from the Yixian Formation (Early Cretaceous) in western Liaoning, China as the earliest normal flower known to date. The flower demonstrates a typical floral organization, including tepals, androecium, and gynoecium. The tepals are spatulate with parallel veins. The stamens have a slender filament, a globular anther, bristles at the anther apex, and in situ round-triangular pollen grains. The gynoecium is composed of two stylate carpels enclosed in a fleshy envelope, and develops into a “hip” when mature. Since the well-accepted history of angiosperms is not much longer than 125 Ma, Callianthus together with Chaoyangia, Archaefructus and Sinocarpus from the Yixian Formation demonstrate a surprisingly high diversity of angiosperms, implying a history of angiosperms much longer than currently accepted.

Wang X, Zheng S (2009). The earliest normal flower from Liaoning Province, China. J. Integr. Plant Biol. 51(8), 800-811.

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