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Review
. 2016 Mar 31:7:402.
doi: 10.3389/fpls.2016.00402. eCollection 2016.

Regulatory Networks in Pollen Development under Cold Stress

Kamal D Sharma  1 , Harsh Nayyar  2
Affiliations
Review

Regulatory Networks in Pollen Development under Cold Stress

Kamal D Sharma et al. Front Plant Sci. .

Abstract

Cold stress modifies anthers' metabolic pathways to induce pollen sterility. Cold-tolerant plants, unlike the susceptible ones, produce high proportion of viable pollen. Anthers in susceptible plants, when exposed to cold stress, increase abscisic acid (ABA) metabolism and reduce ABA catabolism. Increased ABA negatively regulates expression of tapetum cell wall bound invertase and monosaccharide transport genes resulting in distorted carbohydrate pool in anther. Cold-stress also reduces endogenous levels of the bioactive gibberellins (GAs), GA4 and GA7, in susceptible anthers by repression of the GA biosynthesis genes. Here, we discuss recent findings on mechanisms of cold susceptibility in anthers which determine pollen sterility. We also discuss differences in regulatory pathways between cold-stressed anthers of susceptible and tolerant plants that decide pollen sterility or viability.

Keywords: abscisic acid signaling; anther; bioactive gibberellins; cold stress; pollen development; pollen sterility; sugar metabolism.

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Figures

FIGURE 1
FIGURE 1
Genes regulating cell differentiation in early stages (1–5) of anther development. Three cell layers (L1, L2, L3) present in anther primordium divide to form: L1: epidermis (E), L2: endothecium (En), middle layer (ML), tapetum (T), and pollen mother cell (PMC), L3: connective tissue and vascular bundle (C). The development of L2 to En, ML, T, and PMC proceed through several intermediates, e.g., primary parietal cell, archesporial cell, secondary parietal cell, primary sporogenous cell, secondary sporogenous cell. The genes are shown in italics. AG: AGAMOUS, SEP: SEPTELLA, BAM: BARELY ANY MERISTEM, ROXY1/2: Arabidopsis CC-TYPE GLUTAREDOXINS, SPL/NZZ: SPOROCYTELESS/NOZZLE, TCP: TEOSINTE BRANCHED1/CYCLOIDEA/PCF transcription factors, SERK: SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE, EMS1/EXS: EXCESS MICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS, RPK2: RECEPTOR-LIKE PROTEIN KINASE2, DYT1: DYSFUNCTIONAL TAPETUM1, TPD1: TAPETAL DETERMINANT 1, TPL/TPR: TOPLESS/TOPLESS-RELATED.
FIGURE 2
FIGURE 2
ABA biosynthesis in plant cells and its catabolism to phaseic acid. ABA is synthesized from carotenoids in a series of reactions in plastids and cytoplasm. In plastids, the carotenoids are converted to zeaxanthin and zeaxanthin to violaxanthin by enzyme zeaxanthin epoxidase (ZEP). Violaxanthin produces neoxanthin (9-cis-epoxycarotenoid) which is converted to xanthoxin (2-cis,4-trans-xanthoxin) by the oxidative cleavage of neoxanthin by the enzyme 9-cis epoxycarotenoid dioxygenase (NCED; Schwartz et al., 1997; see review by Seo and Koshiba, 2002). Xanthoxin is transported to the cytoplasm where it is converted to ABA by a two-step reaction. ABA is catabolized in cytoplasm to form phaseic acid. Enzyme names are shown in bold. Dotted lines indicate more than one reaction.
FIGURE 3
FIGURE 3
Pathway for ABA accumulation and catabolism in anthers under cold stress. Less amount of ABA accumulated in cold-stressed cold-tolerant anthers compared to susceptible ones, owing to reduced synthesis and increased degradation of ABA. Though, no evidence so far in anthers, ethylene, in plant leaves, positively regulate synthesis of ABA8ox1, 2, and 3, the enzymes required for ABA catabolism. Dotted lines indicate several chemical reactions; the ? Indicates absence of knowledge in anthers; the ∗∗ indicates evidence from leaves; the arrows show the increased and the blocked lines the decreased expression. ABA, abscisic acid; ZEP1, zeaxanthin epoxidase 1; NCED3, 9-cis-epoxycarotenoid dioxygenase3; ABA8ox1, ABA8′-hydroxylase 1; ABA8ox2, ABA8′-hydroxylase 2.
FIGURE 4
FIGURE 4
Cold stress induced reduction in bioactive gibberellins and sugars in cold-susceptible anthers. ABA accumulation in anthers results in pollen sterility and flower abortion by decreasing amounts of reduced free sugars. Lines with arrow show positive reaction. Blocked lines indicate inhibition of chemical reaction. Information within boxes indicate the physiological outcome of reaction. GA12, bioinactive GA; GA4, GA7, bioactive GAs; GA20ox3, GA20-oxidases3; GA3ox1, GA3-oxidases1; ABA, abscisic acid; MST7, monosaccharide transporter 7; MST8, monosaccharide transporter 8, INV4, cell wall invertase4.
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